EVOLUCIÓN

DEPARTAMENTO DE ECOLOGÍA, GENÉTICA Y EVOLUCIÓN
FACULTAD DE CIENCIAS EXACTAS Y NATURALES
UNIVERSIDAD DE BUENOS AIRES

1° CUATRIMESTRE 2015
GUÍA Nº 2

BIOGEOGRAFIA HISTORICA
ESPECIACIÓN
EVOLUCIÓN Y DESARROLLO (EVO­DEVO)
MACROEVOLUCIÓN
EVOLUCIÓN HUMANA
REPASO 2° PARCIAL
 Cronograma 1º Cuatrimestre 2015
Fecha Tema Teórica Fecha Tema TP
Teórica TP
Mi 18/3 Introducción
Vi 20/3 Historia del pensamiento evolutivo
Mi 25/3 Variabilidad genética Ju 26/3 Historia del pensamiento evolutivo I
Vi 27/3 Genética de Poblaciones I Ma 31/3 Historia del pensamiento evolutivo II
Mi 1/4 Genética de Poblaciones II Ju 2/4 Feriado
Vi 3/4 Feriado Ma 7/4 Genética de Poblaciones I
Mi 8/4 Genética de Poblaciones III Ju 9/4 Genética de Poblaciones II
Vi 10/4 Teoría Neutralista Ma 14/4 Genética de Poblaciones III
Mi 15/4 Plasticidad Fenotípica Ju 16/4 Teoría Neutralista I
Vi 17/4 Arquitectura Genética Ma 21/4 Teoría Neutralista II
Mi 22/4 Filogenia I Ju 23/4 Filogenia I
Vi 24/4 Filogenia II Ma 28/4 Filogenia II
Mi 29/4 Filogenia III Ju 30/4 Filogenia III
Vi 1/5 Feriado Ma 5/5 Repaso
Mi 6/5 Repaso Ju 7/5 Libre
Viernes 8/5 1º Parcial Teórico - Práctico
Mi 13/5 Teoría y Realidad de Especie Ma 12/5 Libre
Vi 15/5 Especiación I Ju 14/5 Libre
Mi 20/5 Especiación II Ma 19/5 Biogeografía histórica
Vi 22/5 Especiación III Ju 21/5 Especiación I
Mi 27/5 Especiación IV Ma 26/5 Especiación II
Vi 29/5 Evo Devo Ju 28/5 Especiación III
Mi 3/6 Macroevolución Ma 2/6 Evo Devo I
Vi 5/6 Adaptación Ju 4/6 Evo Devo II
Mi 10/6 Evolución del Sexo Ma 9/6 Macroevolución I
Vi 12/6 Evolución Humana I Ju 11/6 Macroevolución II
Mi 17/6 Evolución Humana II Ma 16/6 Evolución Humana I
Vi 19/6 Evolución Humana III Ju 18/6 Evolución Humana II
Mi 24/6 Repaso Ma 23/6 Evolución Humana III
Vi 26/6 Libre Ju 25/6 Repaso
Ma 30/6 Libre
Miércoles 1/7 2º Parcial Teórico - Práctico
Lunes 13/7 Recuperatorio 1º Parcial
Jueves 16/7 Recuperatorio 2º Parcial

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MÓDULO V: 

BIOGEOGRAFÍA  

HISTÓRICA 
 

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 INTRODUCCIÓN GENERAL  
Ana Liza Tropea 
 
El  trabajo  práctico  a  continuación  constituye  el  inicio  del  segundo  bloque  temático  de  la 
materia en el que se estudiarán los procesos que modelaron la diversidad biológica por encima del 
nivel  poblacional.  Para  ello,  no  sólo  se  requieren  los  conceptos  estudiados  anteriormente 
(procesos microevolutivos) sino que también es necesario introducir nuevos elementos para lograr 
comprender el surgimiento de las especies, sus patrones de variabilidad genética, su distribución 
geográfica y temporal y, sus relaciones de parentesco (nivel macroevolutivo) como resultados de 
un largo proceso histórico, único pero a la vez contingente. En particular, el concepto de tiempo 
geológico  es  de  vital  importancia  para  el  estudio  de  la  historia  de  la  vida  en  la  Tierra,  muy 
diferente a la escala temporal generacional en la que se enmarcan los estudios microevolutivos. 
En  este  nuevo  contexto,  es  interesante  destacar  cómo,  para  inferir  aquellos  procesos  que 
ocurrieron en el pasado y construir escenarios evolutivos, se deben estudiar los correspondientes 
patrones observables en el presente.  
  Como una primera aproximación a esta nueva mirada del mundo vivo, y previo a la lectura 
del módulo, le proponemos la lectura del siguiente material y lo invitamos a reflexionar sobre las 
preguntas a continuación: 
 
S.J.  Gould.  “Los  signos  insensatos  de  la  historia”  en  El  pulgar  del  Panda  (capítulo  2).  Ed.  Crítica. 
1994. Pp.24‐30. 
 
1. ¿Por qué la evolución es una ciencia histórica? ¿Cuáles son las preguntas que se formula? ¿Qué 
metodología/s  utiliza?  ¿Cuál  es  el  estatus  epistemológico  de  las  inferencias  sobre  el  pasado 
evolutivo? 
2.  ¿Qué  son  los  patrones  y  los  procesos  en  el  marco  de  la  biología  evolutiva?  ¿A  qué  hace 
referencia el autor con la frase “Las rarezas, en términos del presente, son las señas de identidad 
de la historia”? Sintetice el ejemplo de las tortugas presentado por el autor. 
3. ¿Qué tipo de información, distinta a la conocida por ud. hasta el momento, se utiliza para inferir 
el pasado evolutivo de las especies, familias u otros clados?  
4.  ¿Por  qué  se  suele  afirmar  que  la  historia  evolutiva  ocurrida  es  “uno  de  muchos  caminos 
posibles”?  
 

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 INTRODUCCIÓN A LA  
BIOGEOGRAFÍA HISTÓRICA 
 
Alexandra M. Gottlieb 
Objetivos 
1‐ Conocer el desarrollo histórico de las ideas en Biogeografía.  
2‐ Familiarizarse con los conceptos utilizados por esta disciplina. 
3‐ Aplicar los conocimientos adquiridos en el planteo de hipótesis que expliquen a través de procesos 
evolutivos, los patrones de distribución geográfica observados. 
 
Introducción 
La Biogeografía es una disciplina histórica que estudia la distribución de los seres vivos en 
el tiempo y el espacio, e incluye temáticas como Geología, Geografía y Biología. 
El padre de la nomenclatura binomial, C. Linneo (1707‐1778), intentó explicar las causas de 
la  distribución  geográfica  de  los  organismos  siguiendo,  en  su  tradición  creacionista  y  fijista,  el 
relato bíblico del Jardín del Edén. Ciertos autores reconocen en el Conde de Buffon (1707‐1788), 
opositor  al  sistema  linneano,  los  comienzos  de  la  Biogeografía.  Fue  su  sistema  alternativo  de 
clasificación  lo  que  le  permitió  a  Buffon  agrupar  los  animales  de  acuerdo  a  su  geografía  y 
organizarlos  en  faunas.  Además,  fue  Buffon  quien  introdujo  el  concepto  de  centros  de  origen 
aunque asociado al creacionismo.  
El  botánico  A.  P.  de  Candolle  (1778‐1841),  en  1820  reconoció  dos  enfoques  en  la 
investigación  biogeográfica:  el  ecológico  y  el  histórico.  Si  bien  antiguamente  estos  eran  dos 
enfoques excluyentes, en la actualidad se reconoce que todo patrón biogeográfico es el resultado 
de  la  combinación  de  ambos  tipos  de  procesos.  La  Biogeografía  Ecológica  analiza  patrones  de 
distribución  a  nivel  local,  de  poblaciones  o  de  especies,  teniendo  en  cuenta  procesos  de 
adaptación  al  ambiente  y  las  relaciones  entre  dichas  poblaciones  o  especies.  La  Biogeografía 
Histórica se ocupa de estudiar a escala global, cómo los procesos históricos que suceden a través 
de  millones  de  años  (v.g.:  la  tectónica  de  placas,  los  movimientos  orogénicos,  los  procesos 
macroevolutivos, etc.) afectan los patrones de distribución de especies y de taxones superiores.  
Los  datos  biogeográficos  fueron  muy  importantes  en el  desarrollo  de  las  ideas  evolutivas 
de C. R. Darwin (1809‐1882) y de A. R. Wallace (1823‐1913). En su libro “Viaje de un naturalista 
alrededor del mundo” (1831‐1835), Darwin se cuestiona acerca de los patrones de distribución de 
plantas y animales, e interpreta los fósiles como restos de los antecesores de los organismos vivos. 
Para Darwin, el clima y las barreras geográficas condicionan y limitan la distribución actual de los 
seres  vivos.  Más  tarde,  Darwin  dedicó  un  capítulo  de  su  “Origen…”  (1859)  a  explicar  muchos 
hechos  biogeográficos  (como  por  ejemplo  el  aislamiento  de  Australia  y  la  evolución  de  los 
marsupiales), al mismo tiempo que el pasado fósil de los organismos actuales fue tratado en otro 
capítulo  de  dicha  obra.  Wallace,  gran  naturalista  inglés  contemporáneo  a  Darwin,  contribuyó 
significativamente  a  la  Biogeografía  con  su  libro  “La  Distribución  Geográfica  de  los  Animales” 
(1876).  Darwin  y  Wallace  consideraban  que  las  especies  se  originaban  en  un  centro  a  partir  del 
cual  algunos  individuos  se  dispersaban  al  azar  y  posteriormente  evolucionaban  por  selección 
natural.  Esta  visión  fue  rebatida  por  Lyell  y  Hooker,  entre  otros,  ya  que  consideraban  poco 
probable la dispersión a larga distancia a través de barreras amplias. En cambio, sostenían que las 
especies  se  habrían  distribuido  a  través  de  grandes  puentes  terrestres  y  continentes,  ahora 

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sumergidos. La tradición de Darwin –Wallace tuvo sus defensores más prominentes en el genetista 
E. Mayr (1904‐2005) y el paleontólogo G. G. Simpson (1902‐1984), entre muchos otros.  
Entre  las  décadas  de  1950  y  1960,  el  paradigma  dominante  en  Biogeografía  era  el 
paradigma  dispersalista  debido  principalmente  a  la  influencia  de  Simpson,  y  a  que  muchos 
biólogos  ignoraban  conceptos  geológicos  como  el  de  Deriva  Continental  (luego  la  Tectónica  de 
Placas).  Justamente  fue  esta  teoría  la  que  dio  sustento  a  la  visión  vicariante  de  la  distribución 
biológica,  opuesta  al  dispersalismo,  antes  mencionado.  No  obstante,  Simpson  distinguió  la 
dispersión  por  medio  de  corredores,  puentes  filtro  y  rutas  al  azar  (o  “sweepstakes”).  Así,  los 
animales  pueden  desplazarse  libremente  en  ambas  direcciones  a  través  de  corredores,  y  en 
consecuencia,  las  regiones  conectadas  tendrían  una  gran  similitud  faunística.  Los  puentes  filtro 
constituían  un  medio  más  selectivo  para  la  dispersión,  ya  que  sólo  ciertas  clases  de  animales 
podría  atravesarlo  y  en  una  dirección.  Las  rutas  al  azar  son  aquellas  que  son  cruzadas 
fortuitamente por algunos organismos al ser arrastrados por las corrientes, o al estar adheridos a 
otros organismos, o simplemente al estar sobre un tronco flotante.  
En  1958  el  botánico  L.  Croizat  (1894–1982)  planteó  que  las  barreras  geográficas 
evolucionaron conjuntamente con las biotas 1 , y que las áreas disyuntas 2  constituyen relictos de 
las  distribuciones  ancestrales.  Croizat  desarrolló  el  método  denominado  panbiogeografía  para 
reconstruir  biotas  ancestrales,  poniendo  énfasis  en  el  análisis  de  los  patrones  de  distribución 
comunes de taxones animales y vegetales, y no en la capacidad de dispersión de cada uno de ellos. 
Este  fue  uno  de  los  primeros  enfoques  que  consideró  a  la  vicarianza  como  un  proceso 
fundamental en la Biogeografía Histórica (ver más adelante).  
Por su parte, W. Hennig (1913‐1976) postuló la existencia de una relación estrecha entre 
las  especies  y  el  espacio  que  ocupa  cada  una  de  ellas.  Con  el  desarrollo  de  la  Cladística  y  su 
aplicación  a  la  Biogeografía,  surgió  la  disciplina  conocida  como  Biogeografía  Cladística.  Este 
enfoque  emplea  cladogramas  para  inferir  la  historia  biogeográfica  de  un  grupo,  en  particular,  el 
interés de esta corriente reside en el estudio de la historia de grupos monofiléticos en el tiempo y 
el espacio. 
 
Deriva Continental y Tectónica de Placas 
El  meteorólogo  A.  Wegener  (1880‐1930)  propuso  en  1915  su  teoría  de  la  Deriva 
Continental, la cual sostenía que los continentes se deslizaban lentamente sobre la superficie de la 
corteza terrestre debido a la fuerza de las mareas. Si bien Wegener no fue el primero en notar que 
muchas  líneas  de  la  costa  (como  América  del  Sur  y  África)  parecieran  encajar  juntas  como  un 
rompecabezas, fue uno de los primeros en proponer que los continentes pudieron haber estado 
ensamblados juntos en algún punto en el pasado formando el supercontinente Pangea (ver Fig. 
1).  Esta  propuesta  fue  apoyada  por  paleontólogos  que  encontraron  fósiles  de  especies  muy 
similares entre continentes ahora separados por una gran distancia geográfica (v.g.: restos de la 
planta fósil Glossopterys en África, Sudamérica, Australia e India; restos de fósiles de un reptil del 
Paleozoico, Mesosaurus, en Brasil y África). Las ideas de Wegener fueron muy polémicas porque 
carecían  de  una  explicación  mecánica  para  el  movimiento  o  deriva  de  los  continentes.  Muchos 
geólogos anti‐movilistas creían que el planeta pasaba por ciclos de calentamiento y enfriamiento, 
lo  que  causaba  la  dilatación  y  contracción  de  las  masas  de  la  tierra.  Los  movilistas,  en  cambio, 
apoyaban  las  ideas  de  Wegener.  Aunque  la  teoría  de  la  Deriva  Continental  fue  posteriormente 
refutada, sentó las bases para el desarrollo de la Tectónica de Placas.  

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 Biotas: conjuntos de taxones que habitan un área geográfica determinada. 
2
 Areas disyuntas: áreas sin continuidad geográfica. 

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FIGURA 1. Esquema cronológico en el que se muestran las masas de tierra emergidas en el Pérmico, 
Triásico, Jurásico, Cretácico y en la época actual, producto del movimiento de las placas tectónicas. 
 
En  los  años  1960  una  serie  de  sismómetros  instalados  para  vigilar  una  prueba  nuclear, 
reveló  que  los  terremotos,  los  volcanes,  y  otros  procesos  geológicos  activos,  se  alineaban  a  lo 
largo de cinturones alrededor del mundo, definiendo los bordes de placas tectónicas. Los estudios 
paleomagnéticos  mostraron  que  el  Polo  Norte  Magnético  vagó  aparentemente  sobre  todo  el 
globo. Esto fue interpretado como que, o bien las placas se movían, o bien el Polo Norte era móvil. 
Excepto los períodos de revocaciones magnéticas en los cuales los Polos Norte y Sur se invierten, 
el Polo Norte se encuentra fijo. Los geólogos y los geofísicos descubrieron que la corteza terrestre 
en el fondo oceánico, tenía registro de estas revocaciones, lo que constituiría una prueba de que la 
litosfera 3  tuvo que estar en movimiento. La evidencia geológica, geofísica y sismológica fortaleció 
la idea de la tectónica de placas. 
Hacia finales de la década de 1960, la comunidad científica aceptó a la Tectónica de Placas 
como un paradigma explicativo coherente acerca de la dinámica del planeta y su interacción con 
los  ecosistemas.  Esta  teoría  explicó  por  ejemplo,  la  existencia  de  marsupiales  en  Sudamérica  y 
Australia  considerando  que  durante  el  Eoceno  (hace  40  millones  de  años,  Ma)  (ver  Fig.  2)  estas 
regiones se encontraban cercanas entre sí y con la Antártica, que para aquel entonces poseía un 
clima cálido. 

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 Litosfera: capa superficial de la Tierra sólida formada por corteza y manto. 

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  La ruptura y separación (es decir, el cambio de posición) de las masas de tierra hace que 
esas regiones estén sometidas a cambios de clima y aislamiento y, en consecuencia, a cambios de 
presión  de  selección  sobre  los  organismos  y  divergencia.  Contrariamente,  las  fusiones  de 
continentes y las migraciones bidireccionales homogeneizan áreas y producen un aumento en la 
competencia  por  el  espacio  y  los  recursos.  La  disposición  de  las  tierras  continentales,  el 
surgimiento  de  islas,  la  apertura  y  cierre  de  plataformas  marinas  y  oceánicas,  etc.,  afectaron 
profundamente la distribución y la historia de los seres vivos.  
 

 
FIGURA 2. Esquema cronológico de los Eones, Eras, Períodos y Épocas geológicas de la Tierra  
(escala cronoestratrigráfica). 
 
Áreas de distribución, áreas de endemismo y centros de origen 
Desde  sus  orígenes  la  Biogeografía  intenta  comprender  por  ejemplo,  por  qué  algunos 
taxones poseen distribución más amplia que otros; o cómo explicar las distribuciones disyuntas de 
los miembros de un mismo taxón; o por qué un taxón es más diverso en ciertas regiones, etc. Por 
distribución  disyunta  se  entiende  aquella  donde  los  miembros  de  un  mismo  taxón  habitan 
localidades muy distantes, sin una continuidad geográfica entre ellas. 
Responder estas preguntas requiere delimitar las áreas de estudio; y para ello se emplean 
dos conceptos fundamentales: área de distribución y área de endemismo.  El área de distribución 
es la región total dentro de la cual se distribuye una unidad taxonómica cualquiera. Se relaciona 
con factores como el clima, el hábitat, la competencia intra e interespecífica, etc. Un parámetro 
importante  del  área  de  distribución  es  su  carácter  continuo  o  discontinuo  (área  disyunta).  La 

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distribución de una especie evolutivamente “nueva” es naturalmente continua, pero los cambios 
climáticos  estocásticos,  las  epidemias  y/o  la  competencia  ecológica  pueden  conducir  a  la 
fragmentación  de  su  distribución  y  a  la  posterior  divergencia  de  las  poblaciones  aisladas 
(especiación  alopátrica).  La  delimitación  de  las  áreas  de  distribución  de  un  taxón  suele  ser  una 
simplificación  de  la  distribución  de  los  organismos  en  la  naturaleza  debido  a  que,  muchas  veces 
éstas representan las localidades donde el taxón ha sido encontrado o coleccionado. Los mapas de 
distribución  pueden  elaborarse  a  partir  de  las  áreas  de  distribución  para  cualquier  nivel  de  la 
jerarquía  linneana  (v.g.:  especies,  familias,  órdenes,  etc.).  Mediante  la  elaboración  de  mapas  de 
distribución,  la  Tierra  fue  dividida  en  ocho  regiones  biogeográficas  para  la  fauna  y  otras  seis 
regiones  para  la  flora.  Por  otro  lado,  los  límites  a  la  distribución  están  determinados  por  los 
atributos ecológicos (nicho fundamental, nicho realizado) e históricos de un taxón. Así una especie 
puede ser ecológicamente apta para vivir en un lugar pero estar ausente porque nunca migró y/o 
logró establecerse. Los cambios climáticos ocurridos en el pasado, como las glaciaciones, trajeron 
como  consecuencia  que  el  rango  de  distribución  de  muchas  especies  del  Hemisferio  Norte  se 
desplazara más hacia el sur por migración. Alternativamente, también pudo haber ocurrido que el 
rango de distribución se contrajera y se desplazara más hacia el sur por la muerte de los individuos 
que habitaban las zonas más frías (sin migración).  
Más  controvertida  es  la  delimitación  del  área  de  endemismo  ya  que  existe  cierta 
dependencia de la escala de estudio y, a su vez, no existe un consenso en la comunidad científica 
acerca  de  su  definición.  Nelson  y  Platnick  (1981)  definieron  áreas  de  endemismo  como  áreas 
relativamente  pequeñas  que  presentan  un  número  significativo  de  especies  que  no  están 
presentes en ninguna otra área. Más tarde, Platnick (1991) la definió como aquella área delimitada 
por  las  distribuciones  congruentes  de  dos  o  más  especies.  Una  especie  es  endémica  (es  un 
endemismo) cuando se presenta en un área muy restringida. Un endemismo puede encontrase en 
el área donde se originó, en cuyo caso decimos que es un neoendemismo. Un paleoendemismo es 
una especie cuya distribución restringida representa sólo una pequeña parte de otra distribución 
anterior  más  amplia,  generalmente  lejos  del  área  en  la  que  surgió  evolutivamente.  Decimos  en 
este caso que la especie ocupa un área relicta o relictual.  
Los  organismos  se  dispersan  desde  su  centro  de  origen  tanto  como  se  lo  permitan  sus 
habilidades y las condiciones del medio. Los datos del registro fósil son esenciales para determinar  
los centros de origen, si bien existen numerosos criterios para su delimitación. Entre los criterios 
más  empleados  se  pueden  mencionar:  (i)  aquel  donde  actualmente  se  encuentra  la  mayor 
diversidad del taxón; (ii) la mayor cantidad de individuos; (iii) los individuos de mayor tamaño; (iv) 
la mayoría de los genes dominantes, etc. 
 
Extinción, dispersión y vicarianza 
La Tierra ha permanecido en un estado de flujo durante 4.000 Ma. A lo largo del tiempo, la 
abundancia  y  diversidad  de  linajes  varió  abruptamente.  Los  linajes  evolucionan  y  radian 
empujando a otros linajes hacia la extinción, o hacia una existencia relictual en refugios protegidos 
(o  microhábitats  adecuados).  Se  han  distinguido  tres  procesos  principales  en  el  tiempo‐espacio 
que pueden modificar la distribución espacial de los organismos: las extinciones, las dispersiones y 
la vicarianza.  
La  extinción  biológica  es  la  desaparición  de  un  taxón  y  representa  la  terminación  de  su 
linaje  o  clado.  La  transformación  de  una  especie  ancestral  en  otra  derivada  se  denomina 
pseudoextinción.  

17
 En  términos  generales,  la  diversidad  ha  aumentado  desde  el  comienzo  de  la  vida.  Sin 
embargo,  el  aumento  se  ha  interrumpido  numerosas  veces  por  las  extinciones  en  masa.  Estas 
implican  una  reducción  de  la  diversidad  biológica  debida  a  la  muerte de  todos  los  individuos  de 
una población local, especie o taxón de rango superior, aproximadamente al mismo tiempo. Las 
extinciones  masivas  están  seguidas  de  periodos  de  radiación  en  los  que  evolucionan  nuevas 
especies que ocupan los nichos vacantes. Por tanto las extinciones moldean el patrón general de la 
macroevolución.  Muchos  investigadores  consideran  que  sobrevivir  a  una  extinción  en  masa  es, 
mayormente, una cuestión de suerte o una lotería, y que las reglas que rigen estos periodos son 
diferentes a las de los tiempos “normales”. Es así que la contingencia jugaría un gran papel en los 
patrones  de  la  macroevolución.  En  clases  posteriores  veremos  cómo  la  modificación  ambiental 
puede ser el impulsor de más cambio evolutivo. 
 El  vulcanismo,  el  impacto  de  asteroides  o  cometas,  o  una  reacción  en  cadena  de  estos 
procesos,  originaron  el  colapso  de  los  ecosistemas  y  el  consecuente  cambio  climático  (v.g.: 
glaciaciones, descenso o aumento de temperaturas, oscilaciones en el nivel de los mares, etc.). Se 
supone que estos procesos han participado como causas de muchas extinciones. 
Los datos paleontológicos indican que las extinciones masivas han sido periódicas, algunas 
más extensas que otras. Son eventos “rápidos” en términos geológicos, es decir, se encuentran en 
el orden de miles a decenas de miles de años. Como ejemplo, podemos mencionar que la biota del 
Mesozoico tuvo su declive y caída durante 1 o 2 Ma, esta cifra representa tan sólo el 0,55% de los 
180 Ma que duró el Mesozoico. Se han registrado numerosas extinciones, aunque cinco de ellas 
son las más destacadas debido a su intensidad en exterminación. La primera extinción (hace unos 
440 Ma) marca el final del Período Ordovícico (ver Fig. 2). El cambio climático se caracterizó por 
ser  severo  y  acompañado  de  un  enfriamiento  global  repentino,  constituyéndose  como  la  causa 
próxima de esta extinción que ocasionó cambios profundos principalmente en la vida marina, pues 
en ese tiempo no existen evidencias de vida terrestre. Se calcula que aproximadamente el 25% de 
las familias de organismos marinos desapareció. La segunda extinción (hace unos 370 Ma) cerca 
del final del Período Devónico, podría haber sido el resultado de cambios climáticos globales. Aquí, 
llegaron a su fin el 19% de las familias. La tercera extinción (hace unos 245 Ma) se produjo hacia el 
final del Período Pérmico (ver Figs. 1 y 2) y se la considera la mayor extinción de la historia de la 
vida en la Tierra (por lo menos hasta ahora!). Evidencias recientes sugieren que el impacto de un 
asteroide,  similar  al  evento  ocurrido  al  final  del  Cretácico,  puede  haber  sido  la  causa  de  esta 
extinción. En esa época también se produjo un descenso mundial del nivel del mar. Se estima que 
desapareció  el  96%  de  todas  las  especies  existentes  (50‐54%  de  todas  las  familias).  La  cuarta 
extinción  (hace  unos  210  Ma),  al  final  del  Período  Triásico,  tuvo  lugar  poco  después  de  la 
evolución  de  los  dinosaurios  y  los  primeros  mamíferos;  sus  causas  aún  son  desconocidas.  Se 
estima que el 23% de las familias de organismos vivientes desapareció. La quinta extinción (hace 
unos 65 Ma) al final del Período Cretácico (en el límite entre los periodos Cretácico y Terciario o 
Límite K/T), es quizás la más famosa y la más reciente de las extinciones. Se ha llegado al consenso 
de  que  este  evento  fue  causado  por  una  colisión  (o  múltiples)  entre  la  Tierra  y  un  asteroide, 
generando un desequilibrio ambiental. Sin embargo, algunos geólogos apuntan a una cadena de 
eventos  físicos  que  perturbaron  severamente  los  ecosistemas.  Aquí,  se  perdió  el  17%  de  las 
familias, y marcó el fin de todos los linajes de dinosaurios, excepto el de las aves, y la desaparición 
de los amonites marinos, así como de muchas otras especies del espectro filogenético y de todos 
los  hábitats.  Con  la  erradicación  de  los  dinosaurios,  los  mamíferos,  confinados  principalmente  a 
nichos insectívoros nocturnos, radiaron ocupando los nichos vacantes. Actualmente, la alteración 
humana  de  la  ecósfera  está  provocando  una  extinción  en  masa  global,  considerada  por  algunos 
científicos como la sexta extinción. 

18
 Como  mencionamos,  la  dispersión  y  la  vicarianza  (ver  Fig.  3)  fueron  originalmente 
consideradas como dos explicaciones mutuamente excluyentes para dar cuenta de la distribución 
disyunta de los grupos de organismos. Actualmente se acepta que ambos procesos ocurren en la 
naturaleza. 
 
  DISPERSION VICARIANZA
  A
  B xyz C p
 
Poblaciones ancestrales y barreras Población ancestral
 
B A C
 
x y p p
  z

 
Dispersión sobre las barreras Aparece una barrera
 
B A C A B
 
x
  x z p1 q
y z
 
  Diferenciación o divergencia de las poblaciones derivadas
  B A C B
A q1 q2
  x1 y p1
x2 z2
z1 p2
  r C
  Más diferenciación
  A B A A C B B C A A
  x1 x2 y z1 z2 q1 q2 r p1 p2
 
 
 
 
 
FIGURA 3. Explicación de la distribución disyunta. Diferencias en el marco de la Biogeografía Histórica entre 
los procesos de dispersión y vicarianza. Modificado de Crisci et al. (2000) y Avise (2000). 
NOTA: las letras mayúsculas indican áreas de distribución; las letras minúsculas indican taxones.  
 
La  explicación  por  dispersión  señala  que  el/los  ancestro/s  común/es  de  los  taxones  con 
distribución  disyunta  se  dispersaron  por  migración  a  partir  de  centros  de  origen  atravesando 
barreras  geográficas  preexistentes,  hacia  donde  se  encuentran  hoy  los  descendientes.  Por  lo 
tanto, la barrera geográfica debería ser más antigua que la disyunción. 

19
 La  explicación  por  vicarianza  sostiene  que  el  ancestro  común  de  los  taxones  con 
distribución  disyunta,  se  encontraba  ampliamente  distribuido  en  un  área  que  comprendía  las 
áreas actualmente disyuntas, las cuales representan restos o relictos de una distribución ancestral. 
La población ancestral se divide en subpoblaciones por el surgimiento de una barrera geográfica 
infranqueable  (v.g.:  el  levantamiento  de  una  cadena  montañosa,  la  ruptura  de  continentes,  la 
subdivisión  de  cuerpos  de  agua,  etc.).  Por  lo  tanto,  la  barrera  no  podría  ser  más  antigua  que  la 
disyunción.  Los  eventos  de  vicarianza  afectan  conjuntamente  a  todos  los  taxones  que  se 
distribuyen  en  un  área,  mientras  que  la  dispersión  afecta  por  lo  general,  a  uno  o  a  unos  pocos 
taxones. 
En  general,  cuando  distintos  grupos  taxonómicos  muestran  distribuciones  correlativas  o 
congruentes,  éstas  fueron  probablemente  producidas  por  vicarianza.  En  cambio,  si  las  diversas 
especies  se  dispersaron  independientemente  de  su  centro  de  origen  entonces  no  tendrán  una 
distribución congruente. Bajo vicarianza, la filogenia de los taxones se corresponde con el orden 
de  separación  de  las  áreas,  mientras  que  bajo  la  hipótesis  de  dispersión  las  áreas  y  los  taxones 
pueden mostrar relaciones históricas más variadas (Fig. 3). 
 
Métodos de la Biogeografía 
La  reconstrucción  que  la  Biogeografía  Histórica  hace  de  los  eventos  del  pasado  puede 
abordarse desde tres perspectivas diferentes: (i) desde los grupos individuales (taxones); (ii) desde 
las áreas de endemismo y; (iii) desde las biotas. 
La mayoría de los métodos biogeográficos emplean cladogramas como herramienta básica 
de inferencia de relaciones históricas. Los biogeógrafos testean sus ideas mediante el estudio de 
los patrones de división (cladogénesis) de un grupo de organismos y su correspondencia, o no, con 
la historia geológica y geográfica de la región en la que vivía dicho grupo. Para esto, construyen un 
cladograma  de  áreas  (ver  Fig.  3)  reemplazando  los  nombres  de  los  taxones  terminales  por  las 
áreas  de  endemismo  donde  se  distribuyen.  Este  procedimiento  es  simple  si  cada  taxón  es 
endémico  de  un  único  área  o  si  cada  área  posee  un  único  taxón.  Cuando  este  no  es  el  caso,  es 
decir  cuando  los  taxones  están  ampliamente  distribuidos  o  cuando  existen  distribuciones 
redundantes  y/o  hay  áreas  ausentes,  deben  aplicarse  ciertas  reglas  metodológicas  para  resolver 
los cladogramas. Como mencionamos anteriormente, si la cladogénesis fue causada por procesos 
geológicos (vicarianza), la filogenia del grupo reflejará la secuencia definida de eventos tectónicos. 
Al  examinar  cladogramas  de  otros  taxones  de  las  mismas  áreas,  éstos  deberían  ser  congruentes 
(deberían coincidir en el orden de ramificación). Este análisis sólo es válido cuando se trabaja con 
grupos monofiléticos, lo que implica que la Biogeografía se sustenta en clasificaciones naturales. 
La metodología general puede resumirse como sigue: 
1. obtención del cladograma del grupo en estudio; 
2. proyección del cladograma sobre un mapa de áreas de distribución; 
3. individualización  del  centro  de  origen  del  grupo  mediante  la  aplicación  de  reglas 
específicas; 
4. formulación de una hipótesis sobre la biogeografía del grupo; 
5. confrontación  de  la  hipótesis  con  la  geología  del  área  y  otras  fuentes  de  datos 
independientes. 
 

20
 Existen al menos nueve metodologías básicas. Algunos de estos métodos asumen que sólo 
operó  el  proceso  de  dispersión,  mientras  que  otros  métodos  consideran  también  a  la  vicarianza 
como proceso que modeló el patrón de distribución observado. Al mismo tiempo, ciertos métodos 
reconstruyen  la  historia  de  biotas;  otros  reconstruyen  la  distribución  de  biotas  individuales  o  la 
historia de las áreas; mientras que otros trabajan sobre biotas y áreas conjuntamente. Respecto al 
rango  taxonómico  de  aplicación,  la  Filogeografía  es  la  única  metodología  que  se  aplica  al  nivel 
poblacional.  Las  metodologías  restantes  trabajan  a  nivel  de  especies  o  de  taxones  de  rango 
superior.   
La  Biogeografía  Cladística  basa  sus  inferencias  en  el  supuesto  que  establece  que  los 
miembros  más  primitivos  de  un  taxón  se  hallan  más  cercanos  al  centro  de  origen.  A  su  vez,  la 
hipótesis  nula  contra  la  cual  se  testean  los  resultados  es  que  la  distribución  de  grupos 
taxonómicos es determinada por eventos de vicarianza dentro del rango de la especie ancestral; 
mientras  que  generalmente  la  hipótesis  alternativa  propone  que  la  distribución  observada  está 
determinada por dispersión.  
 
Lectura adicional (optativa) 
En la página de la materia encontrará los siguientes trabajos: 
1‐ Webb DS (2006) The Great American Biotic Interchange: patterns and processes. Ann. Missouri Bot. 
Gard. 93: 245–257. 
2‐ Marshall LG, Webb DS, JJ Sepkoski Jr, Raup DM (1982) Mammalian evolution and the Great American 
Interchange. Science 215:  1351‐1357. 
 
Bibliografía Consultada 
Avise  JC.  (2000).  Phylogeography.  The  history  and  formation  of  species.  Harvard  Univ.  Press.  London 
England.  
Beardsley PM, Getty SR  & P Numedahl (2009)  Explaining Biogeographic data: Evidence for Evolution. The 
American Biology Teacher 71 (2): 5‐9. 
Crisci  JV,  Katinas  L,  Posadas  P.  (2000).  Introducción  a  la  teoría  y  práctica  de  la  Biogeografía  Histórica. 
Sociedad Argentina de Botánica. Pp.169 
Damborenea  MC  &  Cigliano  MM.  (2006).  Cladística  y  sus  aplicaciones  en  Biogeografía  Histórica  y  co‐
evolución  (capítulo  13).  En:  Sistemática  Biológica:  fundamentos  teóricos  y  ejercitaciones.  Lanteri 
AA, Cigliano MM Eds. 203‐219. Universidad Nacional de La Plata. 
Eldregde N. (1989) Life Pulse: Episodes from the story of the fossil record. FOF Publication. NY, UK, pp. 246. 
Fernández‐López  SR  (2000).  La  naturaleza  del  registro  fósil  y  el  análisis  de  las  extinciones.  Coloquios  de 
Paleontología 51: 267‐280. 
Nelson GJ, Platnick NI (1981) Systematics and biogeography: cladistics and vicariance. Columbia Univ. Press, 
NY. 
Platnick NI (1991) On areas of endemism. Australian Systematic Botany 4: 11‐12. 
Ridley M. (2004). Evolutionary Biogeography (Capítulo 17). En: Evolution. 3rd Ed. Blackwell Publishing. 
 
 
 

21
 DESARROLLO DEL TRABAJO PRÁCTICO 
 
PRIMERA PARTE 
Como  se  mencionó  anteriormente,  la  noción  de  “profundidad  del  tiempo  geológico” 
constituye  un  eje  fundamental  sobre  el  que  se  articulan  las  inferencias  o  reconstrucciones  del 
pasado  evolutivo  de  las  especies  o,  taxones  de  orden  superior.  Sin  embargo,  resulta  muy  difícil 
incorporar  dicha  escala  de  tiempo  dado  que  excede  ampliamente  los  rangos  temporales 
compatibles con la historia humana y, más aun, con la esperanza de vida de nuestra especie. 
En  un  esfuerzo  por  hacer  comprender  la  velocidad  relativa  con  que  se  sucedieron  las 
diversas  etapas  desde  que  se  formó  el  Universo,  Carl  Sagan,  el  conocido  astrónomo  de  la 
Universidad  de  Cornell,  en  su  libro  Los  Dragones  del  Edén,  ha  incluido  lo  que  él  llama  "El 
Calendario  Cósmico":  supongamos  que  pudiéramos  comprimir  los  quince  mil  millones  de  años 
que  han  transcurrido  desde  la  Gran  Explosión  hasta  nuestros  días  en  un  sólo  año.  Así,  cada  mil 
millones de años corresponderían a 24 días del Calendario Cósmico, en tanto que un segundo del 
año cósmico equivaldría a 475 vueltas de la Tierra alrededor del Sol. A esta escala, la evolución del 
universo transcurre a una gran velocidad. Sin embargo, para poder completar la historia de la vida 
en nuestro planeta y el desarrollo de la historia en esta perspectiva, Sagan dividió este calendario 
en  tres  etapas,  las  fechas  precámbricas,  el  mes  de  diciembre  y  finalmente  el  último  día  del  año 
cósmico (ver figura 4). 
El  Calendario  Cósmico  fue  elaborado  a  partir  de  la  información  más  confiable  con  que 
contamos  hoy  en  día  y  es  posible  sin  lugar  a  duda  que  admita  modificaciones  a  medida  que  se 
profundice el conocimiento científico. Sin embargo, no cambiará la conclusión de que somos parte 
de  un  proceso  de  evolución  que  se  inició  con el  origen  mismo  del  Universo,  además,  como  dice 
Sagan,  la  conciencia  de  que  las  grandes  hazañas  del  hombre  ocupan  apenas  unos  cuantos 
segundos de este primer año.  
 
1.1. A partir de la figura 4, destaque los principales hechos de interés para la biología evolutiva. 
¿En qué porción del tiempo han ocurrido dichos eventos? 
 
1.2. ¿En qué momento surge la vida? ¿Y nuestra especie? 
 

22
Figura 4: Calendario Cósmico, Carl Sagan

23
SEGUNDA PARTE 
Usted  es  un  investigador  interesado  en  realizar  un  estudio  biogeográfico  de  las  faunas  de 
mamíferos de América del Norte y del Sur de los últimos 12 millones de años. 
 
2.1.  ¿En  qué  período  geológico  se  enmarca  este  estudio?  ¿Cómo  se  ubicaban  las  placas 
continentales  de  la  actual  América  en  dicho  período?  Utilice  las  figuras  1  y  2  de  la 
introducción teórica y la figura 5 de la parte práctica. 
2.2. A partir del esquema de la figura 6,  complete la tabla 1 con:  
 ‐ el número de registros de fósiles de los linajes indicados en cada uno de los 6 sitios; 
 ‐ la sumatoria del número de registros y la datación aproximada del fósil más antiguo, para 
cada una de las dos regiones, tanto América del Norte como América del Sur. 
 
3. Responda el siguiente cuestionario: 
3.1. Considerando el rango de 11 a 4 millones de años antes del presente (AP), indique las 
familias de mamíferos endémicas para Norteamérica y Sudamérica. 
3.2.  Indique  el  tiempo  aproximado  de  arribo,  o  introducción,  de  animales  endémicos  de 
Sudamérica en Norteamérica y el tiempo de arribo de los linajes endémicos sudamericanos 
en Norteamérica. ¿En qué datos se basó? 
3.3. ¿Cómo explicaría el arribo de animales endémicos sudamericanos a América del Norte (y 
viceversa)?  
3.4.  Examine  el  registro  del  linaje  de  los  rinocerontes.  ¿En  qué  rango  de  tiempo  hay 
evidencias  de  estos  organismos?  ¿Qué  inferencias  puede hacer  acerca  de  la  historia  de  los 
rinocerontes? Proponga hipótesis alternativas. 
3.5. ¿Cuál es la evidencia fósil más temprana del linaje de los mamuts? ¿Cómo explicaría la 
ocurrencia repentina de mamuts en el registro fósil? ¿Hay evidencias de estos organismos en 
Sudamérica? 
3.6.  Para  un  tiempo  geológico  dado,  ¿considera  que  cada  sitio  muestra  todos  los  animales 
que se desarrollaron allí? Justifique. 
 
 

 
FIGURA 5. Formación del istmo de Panamá. 
 

24
FIGURA 6. Esquema de registros paleontológicos de seis secciones geológicas. Los fósiles de 12 familias de mamíferos identificados por sus
iniciales, se presentan en función de la edad geológica (Ma, millones de años).

ESTADOS UNIDOS MÉJICO COLOMBIA ARGENTINA

Ma Florida Arizona Nuevo Méjico
0
O M O Pu F E E A P Gl Cm
F Cm P Cm E M C Gl O P
M P M A P F O F
2 Gl E P M Gl A Cm E
Pu Cp P Cp P Cp E C P Cp
A F C P O P Gl
F Cm E C P Cp O
4 C Pu A Cp
F F A O Cp Pu
Cm E E E R A P Cp O
F E E O Pu
6 E C Cm R Cp Pu P
R C E F Cm Gl P A
F R P O
E F R E Cp P
8 Cm C R E E P A Pu
R P A Gl
Cm E C O Pu
Cm C Gl Pu P
10 F O Cp O
C R
F Cp A

12

25
TABLA 1.

ESTADOS UNIDOS MÉJICO COLOMBIA ARGENTINA

Florida Arizona Nuevo NORTEAMÉRICA SUDAMÉRICA
Méjico
Registros Registros Registros Registros Registros Datación Registros Registros Registros Datación
Organismos totales (Ma) totales (Ma)
Armadillo (A)

Camélido (Cm)

Cánido (C)

Capibara (Cp)

Equido (E)

Félido (F)

Gliptodonte (Gl)

Mamut (M)

Opósum (O)

Perezoso (P)

Puercoespín (Pu)

Rinoceronte (R)

26
 

Concepción  diagramática  de  Simpson  (1940)  sobre  la  migración  a  través  de  puentes. 
(Traducción: Los puentes NO: 1) permiten que solo pase un tipo de animal, 2) permiten 
viajar en una única dirección y 3) transportan fauna completamente desbalanceada.) 

27
Ejercitación adicional 
Entre  la  fauna  del  archipiélago  de  Los  Cocos  se  encuentran  los  caracoles  terrestres  del  género 
Gouldiana.  Estos  caracoles  están  presentes  en  casi  la  totalidad  de  las  islas  que  conforman  el 
archipiélago pero se discute cómo llegaron a poblarlas. 
 
Sabiendo: 
‐ Que la distribución de las especies reconocidas en el archipiélago es la informada en la Figura 1. 
‐ Que algunas especies de caracoles presentan bandas coloreadas es su concha. 
‐ Que todas las especies de caracoles son vegetarianos. 
‐ Que la filogenia más reciente y completa del grupo es la informada en la Figura 2. 
‐ Que durante la última glaciación el nivel del mar estaba 100 metros por debajo del nivel actual, y 
todas las islas conformaban una masa terrestre denominada Antiguos Cocos. 
 
Responda: 
a.  ¿Qué  proceso  biogeográfico  considera  compatible  con  el  patrón  de  distribución  de  especies 
entre islas? Justifique. 
 
b. ¿Qué evidencia o prueba adicional aportaría mayor soporte a su hipótesis? 
 
c.  ¿Cuál  es  el  modelo  geográfico  de  especiación  que  explicaría  la  evolución  de  las  diferentes 
especies de caracoles entre las distintas islas? Justifique brevemente. 
 
d.  Utilice  un  modelo  alternativo  para  explicar  la  divergencia  y  especiación  dentro  de  las  islas  y 
enuncie las condiciones necesarias para que este modelo pueda aplicarse. 
 
e. Bajo el modelo que Ud. postuló en c): ¿cómo ocurrió la divergencia genética entre las especies? 
¿Cuántos genes y qué tipo de caracteres fueron los involucrados?    
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

28
  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Figura 1: Archipiélago de Los Cocos 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Figura 2: Reconstrucción filogenética a partir de secuencias de genes nucleares y mitocondriales.  

29
30
 

 
 
 
 
 
 
 
 

MÓDULO VI: 

ESPECIACIÓN 

 
 

31
32
 SEMINARIO I: REALIDAD Y CONCEPTOS DE ESPECIES 
Marcela Rodriguero & Abel Carcagno 
 

En este seminario se discutirá la existencia de las especies como entidades reales y válidas 
como objeto de estudio. Además, se reflexionará sobre los distintos conceptos de especie y 
los criterios, principalmente metodológicos, ligados a su adopción. 
 
Nota:  Se  recomienda  especialmente  la  lectura  crítica  del  trabajo  “The  meaning  of  species 
and  speciation:  a  genetic  perspective”,  de  Alan  Templeton  (versión  traducida  al  español), 
disponible en http://www.ege.fcen.uba.ar/materias/evolucion/material.htm 
 
Parte I: Realidad de las especies 
• Hey J. 2001. The mind of the species problem. Trends in Ecology and Evolution 16 (7): 326‐
329. 
•  Hey  J.,  Waples  R.S.,  Arnold  M.L.,  Butlin  R.K.  &  Harrison  R.G.  2003.  Understanding  and 
confronting  species  uncertainty  in  biology  and  conservation.  Trends  in  Ecology  and 
Evolution 18 (11): 597‐603. (Fragmento). 
 
1‐ Para comenzar a discutir: ¿cree Ud. en la realidad de las especies?  
2‐ ¿En qué consiste el “problema de las especies”?  
3‐ De acuerdo a lo discutido en el item anterior, en las clases teóricas y a lo que le dicta el 
sentido  común…  ¿cuáles  son  los  posibles  significados  que  pueden  otorgarse  a  la  palabra 
“especie”?  
4‐ De acuerdo a lo discutido en los item 2 y 3 anterior, ¿qué clases de ambigüedad pueden 
desprenderse  de  las  definiciones  de  especie  enunciadas  y  cómo  se  podría  confrontar  este 
problema?  
5‐  ¿Cuál  es  el  resultado  del  proceso  evolutivo  según  Hey  (2001)  y  de  qué  manera  podría 
abordarse  su  estudio?  ¿Qué  problemas  podrían  surgir  al  encarar  un  trabajo  de  esta 
magnitud?  
6‐  ¿Cree  que  existe  alguna  correspondencia  entre  las  especies  y  los  grupos  evolutivos? 
Fundamente su respuesta. 
 
Parte II: Conceptos de especie 
• Gross L. (2007) Who needs sex (or males) anyway? PLoS Biology 5(4): e99. 
• de Meeûs T., Michalakis Y. & Renaud F. (1998) Santa Rosalia revisited : or why are there so 
many kinds of parasites in “the garden of earthly delights”? Parasitol. Today 14(1): 10‐
13. 

33
•  “Species  in  Time”,  fragmento  del  miniensayo  “The  Species  concept”,  de  Richard  Cowen 
(Departamento de Geología de la Universidad de California Davis). 
•  Schlick‐Steiner  B.C.,  Seifert  B.,  Stauffer  C.,  Christian  E.,  Crozier  R.H.,  Steiner  F.m.  2007. 
Without  morphology,  cryptic  species  stay  in  taxonomic  crypsis  folowing  discovery. 
Trends Ecol. Evol. 22(8): 391‐392. 
 
7‐ ¿Cuál es la principal característica de la clase Bdelloidea y cómo repercute en la aplicación 
del CBS a este taxón? 
8‐  De  acuerdo  al  Concepto  Biológico  de  Especie…  ¿cuántos  grupos  esperaría  encontrar 
dentro de la clase? ¿Cómo podría explicar entonces la ocurrencia de discontinuidades dentro 
de Bdelloidea? 
9‐  ¿Qué  otro  concepto  podría  explicar  a  las  categorías  existentes  dentro  de  esta  clase? 
Discuta los potenciales problemas de cada alternativa propuesta. 
10‐ Enuncie al menos dos características que dificulten la aplicación del Concepto Biológico 
de Especie a los organismos parásitos. 
11‐  De  acuerdo  a  los  problemas  analizados  y  a  los  conceptos  que  Ud.  conoce…  ¿cuáles 
aplicaría  a  las  discontinuidades  identificadas  dentro  de  los  grupos  de  organismos  que 
exhiben un modo de vida parasitario? (Como antes, considere las posibles  desventajas). 
12‐ Teniendo en cuenta la diversificación de los organismos estrictamente asexuales y de los 
parásitos,  por  ejemplo…  ¿Considera  al  sexo  como  a  una  condición  sine  qua  non  para  el 
origen de los grupos evolutivos? 
13‐  ¿Cuál  es  el  problema  que  encaran  los  paleontólogos  al  incluir  el  factor  tiempo  en  el 
estudio  de  la  diversidad  biológica  y  cómo  redunda  esto  en  la  aplicación  del  Concepto 
Biológico de Especie a organismos extintos? 
14‐ ¿Cómo solucionaría Ud. estos inconvenientes? (No olvide discutir ventajas y desventajas 
de sus propuestas). 
15‐  ¿Cómo  repercute  la  existencia  de  las  especies  crípticas  en  el  concepto  de  especies 
morfológico? ¿Puede nombrar otro inconveniente para la aplicación de este concepto? 
 
Preguntas unificadoras 
16‐  De  acuerdo  a  lo  discutido,  está  en  condiciones  de  contestar  la  siguiente  pregunta: 
¿Cuáles son las dificultades que impiden la adopción de un único concepto de especie? 
17‐  ¿Cree  que  algún  día  se  arribará  a  una  “solución  radical  al  problema  de  las  especies” 
(Ghiselin 1974)? 
18‐ Explique la siguiente afirmación: “… [como el Concepto Biológico de Especie] se enfoca 
en  el  resultado  y  no  en  el  proceso,  ha  resultado  perjudicial  para  los  estudios  de  los 
mecanismos de especiación…”. 
19‐ ¿Qué fuerza/s mantiene/n la cohesión dentro de cada “especie”, y a la vez  permite/n 
que estas se conserven como entidades discretas? ¿Qué concepto de especie hace alusión a 
esta cuestión? 

34
326 Opinion TRENDS in Ecology & Evolution Vol.16 No.7 July 2001

The mind of the result was an apparently unpublishable ‘species’

manifesto. Although it attracts some readers on the
Internet, it has so far failed to inspire the groundswell

species problem of consensus that I once felt it deserved.

A striking commonality of these numerous
definitions is that, with few exceptions, they are clearly
not to be interpreted as the different meanings of a set
Jody Hey of homonyms, but rather as competitors for the single
best meaning. There seems to be something about the
perceived extensions and the intensions (the ideas in the
The species problem is the long-standing failure of biologists to agree on how we minds) that are shared between these many definitions.
should identify species and how we should define the word ‘species’. The This commonality can also be appreciated whenever two
innumerable attacks on the problem have turned the often-repeated question or more evolutionary biologists use the word ‘species’
‘what are species?’ into a philosophical conundrum. Today, the preferred form of in scientific conversations. This happens frequently,
attack is the well-crafted argument, and debaters seem to have stopped inquiring usually with a seamless exchange of ideas. Despite
about what new information is needed to solve the problem. However, our many different notions of ‘species’, and uncertainty and
knowledge is not complete and we have overlooked something. The species disagreement over them, the word almost always gets
problem can be overcome if we understand our own role, as conflicted passed back and forth with tacit understanding. This
investigators, in causing the problem. apparent consensus thrives until that awkward moment
when someone asks another what he or she means by
Have enough words been said and written on the ‘species’, at which point the consensus and the shared
subject of what species are? How many evolutionary thread of understanding can evaporate. It is as if on
biologists sometimes wish that not one more word, in one hand we know just what ‘species’ means, and on
speech or text, be spent on explaining species? How the other hand, we have no idea what it means.
many biologists feel that they have a pretty good I cannot think of any other word that garners as
understanding of what species are? Among those who much lexicographical attention as ‘species’. Certainly
do, how many could convince a large, diverse group of evolutionary biology is full of difficult ideas, and words
scientists that they are correct? such as ‘adaptation’ and ‘fitness’ often deserve and
At this last and most essential task, many great receive a lot of attention5. But those discussions are
scientists have tried and failed. Darwin, Mayr, Simpson broadly conceptual and do not focus on definitions per se,
and others have taught us about species, but none has the way that ‘species’ debates do. Of course, many
been broadly convincing on the basic questions of what words resemble ‘species’ in having fuzzy extensions
the word ‘species’ means or how we should identify (i.e. wide-ranging, sometimes vague referents) and
species. For its entire brief history, the field of some are the subject of debates over definitions. For
evolutionary biology has simply lacked a consensus on example, the definition of ‘drought’ can matter greatly
these two related questions. Indeed, there was broader for public policy6,7, and the meaning of ‘disease’
consensus before Darwin. Given the once widespread generates both philosophical and practical debates8.
acceptance of an essentialist view of species, perhaps But neither of these examples, nor any others that I can
Linnaeus was our most capable and persuasive species think of, resemble ‘species’in being the subject of so
pundit1, although he was wrong, of course. Darwin much attention that is both broadly theoretical and so
killed species essentialism, but in so doing, he fostered narrowly focused on achieving the best single definition.
rather than settled questions about what species really Consider the parallels between the motives and
are. Since then, the species problem has beseeched us the species concepts of two of our most practiced
like the mythical sirens. Again and again, we pose and ‘species’ definers. Ernst Mayr has been tweaking the
seek an answer to the question ‘what are species?’. Biological Species Concept for decades1,9,10. Joel
Other allegories seem apropos as well2: consider that the Cracraft has been doing exactly the same thing with a
species problem is like a sword, thrust by Darwin into version of the Phylogenetic Species Concept11–13. Both
the stone, and left for us to yank upon with scientists are exceptional evolutionary biologists and
determination and futility. The often dreamed of ornithologists. Both argue that species are real and
magic is a compelling definition of ‘species’ that fits our distinct entities in nature and that we need a succinct
understanding of the causes of biological diversity and species concept that sums up the way in which they
that leads us to identify species accurately and agreeably. exist, and they both argue that we need a species
concept that helps investigators to identify such
The focus on definitions things10,12–14. In short, they both want to understand
Jody Hey
Dept of Genetics, Rutgers
A recent listing found two dozen different definitions real species and to be able to identify them, and both
University, Nelson of ‘species’ (i.e. species concepts, Box 1), most of which perceive a crucial role for a pithy definition. Despite
Biological Labs, 604 were invented within the past few decades3; and, since these similarities, they are led to dissimilar
Allison Rd, Piscataway,
then, new ones have continued to appear4. I was also definitions, and neither finds much utility in the
NJ 08854-8082, USA.
e-mail: seduced by the ‘what are species?’ question, and once other’s concept. Of course, their concepts have some
jhey@mbcl.rutgers.edu devoted much time to puzzling over definitions. The compatibility with each other and with evolutionary

http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02145-0

35
 Opinion TRENDS in Ecology & Evolution Vol.16 No.7 July 2001 327

Box 1. Species conceptsa

• Agamospecies Concept • Internodal Species Concept • Reproductive Competition Concept*

• Biological Species Concept* • Morphological Species Concept • Successional Species Concept
• Cladistic Species Concept • Non-dimensional Species Concept • Taxonomic Species Concept
• Cohesion Species Concept* • Phenetic Species Concept Reference
• Composite Species Concept • Phylogenetic Species Concept a Mayden, R.L. (1997) A hierarchy of species concepts:
• Ecological Species Concept* (Diagnosable Version)* the denouement in the saga of the species problem.
• Evolutionary Significant Unit* • Phylogenetic Species Concept In Species: the Units of Biodiversity (Claridge, M.F.
et al., eds), pp. 381–424, Chapman & Hall
• Evolutionary Species Concept* (Monophyly Version)
• Genealogical Concordance Concept • Phylogenetic Species Concept *Concepts that make reference to biological
processes (e.g. reproduction and competition) that
• Genetic Species Concept* (Diagnosable and Monophyly Version)
occur among organisms within species (and less so
• Genotypic Cluster Concept • Polythetic Species Concept between species) and that contribute to a shared
• Hennigian Species Concept* • Recognition Species Concept* process of evolution within species.

theory15, but, for those needing the single best By taking this approach, we are not acting like
definition, that is beside the point. scientists. We are acting like some philosophers,
It is best to be plain about these and other similar particularly Aristotle, who addressed and supposedly
efforts to find a definition that dispels the species solved questions of the natural world by giving words
problem. Descriptive definitions are not great containers to intuited essences; that is, by making up definitions18.
of knowledge and they are not great tools for arbitrating
the natural world. Individually, descriptive definitions An untapped source of information
are but small bundles of information or theory, and if Fortunately, we can learn rather a lot from our
they seem to be of any great aid in arbitration, it is unscientific behavior. Not only do we see in it a sure sign
because they are backed up by a far larger fund of that we lack information about the species problem, but
knowledge. In short, if you have got the knowledge we also find a place in which to look for that information.
then the definitions are the easy part and fall readily That place is within ourselves, in the ways that our
into place. If your knowledge is incorrect or incomplete, minds handle questions about species. To be clear, I am
no amount of wordplay will set it right. Those who have saying that one source of new information and insight,
tried to puzzle out the species problem by focusing on to which we should turn if we are to solve the species
definitions are missing something, and that something problem, is our own behavior. Note that several authors
is bigger and more important than any definition. have concluded that we demand too much of species
But how could our knowledge, upon which the species concepts and that some of our demands are inherently
debates have been built, be missing something? Do not contradictory2,19–22. It is but a short step (and a great leap)
evolutionary biologists know of genetics, fossils, to cast such arguments in terms of the question: what is
geography and the vast organismal diversity that exists it about our minds and our motives that mislead us?
on our planet? Does not every evolutionary biologist Once we are introspective in this way, we
know, from theory and mountains of evidence, that immediately obtain one clear answer to the question
evolution gives rise to organismal groups, within which ‘what are species?’. In our minds and in our language,
individuals are similar and closely related, and between species are categories. That is to say, the names for
which divergence can and does accrue? But, despite species and the usage of those names take an entirely
these intellectual riches, we must recognize that our conventional syntactical role that is taken by all
knowledge of species has not been sufficient to resolve categories. Just as ‘planet’ is the name of a category,
the species problem. Our obdurate debates16 and our and appears as a predicate in sentences (e.g. ‘The
misplaced ambitions for ‘species’ definitions are a slap Earth is a planet.’), so ‘polar bear’ is also a category
in the face – they forcefully remind us that there are and a frequent predicate in sentences. Whatever else
some things that we just do not know about or they are, categories are things in the mind and in our
understand sufficiently to describe them adequately17. language, and they are used for organizing our
The awkward juxtaposition of apparent ignorance and thoughts and language about organismal diversity.
seemingly complete knowledge can also be seen in one
of our most common modes of explanation. Consider the Taxa
now traditional method in which the nature of species and Of course, ‘species are categories’is just a starting point,
the meaning of ‘species’ are addressed first by summing but it is one that helps us to tap into a large tradition of
up the inadequate state of affairs, followed by an exertion inquiry on the connections between categories in the
of pure reason. There are dozens, if not hundreds, of mind and things in the real world17,23–26. Categories are
elegant articles that employ this approach. These articles motivated by recurrent observations about the world27.
are permeated with the presumption that new argument, Humans are great observers of patterns of repetition,
and not new information, will settle the question. Species and we devise our categories as a response. These so-
pundits do not ask ‘what new information do we need?’. called ‘natural kinds’ are in our heads, but they are also

http://tree.trends.com

36
328 Opinion TRENDS in Ecology & Evolution Vol.16 No.7 July 2001

out there in the world, in some way. For example, frozen Fundamental conflicts
wispy crystals of water sometimes fall to earth in great Now let us compare and contrast the idea of a species
numbers and we identify them as snowflakes. The taxon with the idea of a species as an evolutionary
‘snowflake’category exists in our minds, but in some group. To begin with, these two meanings of ‘species’
sense it is also a feature of the world outside ourselves, a refer to things that are fundamentally and ontologically
world that is disposed to repeatedly generate individual dissimilar. To the extent that instances of either of them
falling wispy crystals of water. Each of the species that exist, they do so in very different ways. An evolutionary
we identify is a category, but it is also a natural kind that group is an entity, somewhat discrete in space and time,
exists as a pattern of recurrence in the world. We call and capable of changing and being acted upon30–34. It
these natural kinds ‘taxa’ and, whatever else they are, does not matter that its parts (individual organisms) can
there is no escaping the fact that we identify them first move around with respect to one another, and it does
on the basis of recurrent patterns that we find in nature. not matter that it is not entirely distinct and separate
What does it take to make such a species taxon? One from other such entities. Evolutionary groups share
answer is that it does not take much: given a simple these properties with all sorts of other entities, and the
observation of a few organisms that seem similar to one arguments about their ontology (the way they exist) are
another, and different from others, and a biologist is off fairly simple, at least compared with those for categories
and thinking about devising a new taxon. Another and taxa32. Whether natural kinds exist is an often-
answer is that it varies tremendously with the debated question, but even if they do, it is an altogether
observer. Not surprisingly, biologists cannot agree on different sort of existence than for individual entities35–37.
how distinct a seemingly new pattern must be to Another major difference between the two viewpoints
motivate a new named category. These lumper/splitter is the role that distinction plays in their existence. We
debates go round and round, much as they have for recognize and devise species taxa pretty much as a direct
hundreds of years. Consider the situation with birds, result of having perceived a seemingly distinct pattern of
which for people are probably the most observable recurrence. We devise taxa because they usefully serve
animals on the planet. Conventional classifications our drive to categorize things, and so their very existence
place the number of bird species worldwide at around (such as it is) goes hand-in-hand with their perceived
9000. But some feel that a proper evaluation would degree of distinction. By contrast, evolutionary groups
yield a count closer to 20 000 (Refs 28,29). exist regardless of our recognition of them, and they
So now we have one answer to ‘what are species?’. might or might not be distinct. Note that as much as
They are categories and, more particularly, they are the word ‘group’ can be taken to convey distinction, in
named natural kinds of organisms: taxa. We also fact the world is full of things that exist and are not at
know what causes them, and that they are the result all distinct. Some that we are familiar with are clouds,
of two processes: (1) the evolutionary processes that populations, and ecosystems. Since the early 20th
have caused biological diversity; and (2) the human century, evolutionary biologists have been well trained
mental apparatus that recognizes and gives names to in the many ways that evolving groups of organisms
patterns of recurrence. might not be distinct. Genes can be and are exchanged
at varying rates between such groups, and there are
Evolutionary groups myriad ways that levels of gene exchange can be
For many biologists, however, species taxa are entirely structured to create groups within groups38.
inadequate for many of the purposes for which we use Finally, consider our very different motivations
‘species’. These biologists are interested in the causes towards the different usages of ‘species’. Names of taxa
of species, not our mental contributions to taxa, but are among children’s very first words (not the technical
rather the evolutionary processes that create patterns jargon, of course, but words like ‘dog’and ‘bird’) and
of biodiversity. Of the many concepts listed by Mayden3, adult biologists employ taxa in exactly the same manner:
many either strongly imply or explicitly state that a that is, as named categories. Consider too that all
species is a group of related organisms, one that is human societies have taxa that are part of taxonomic
enjoined by evolutionary processes that go on within systems that share some remarkable similarities with
it, and that is separate from other groups because of each other and with those systems used by professional
the absence of shared evolutionary processes with biologists25,39. Surely humans have been devising and
those other groups (Box 1). It is these theoretical ideas using taxa ever since their ancestors evolved the capacity
of evolving groups that descend fairly directly from for language. If there is one thing at which our brains are
Darwin’s teachings, and they mark a drastic adept, it is recognizing and devising different kinds of
departure from purely categorical or taxonomic ideas organisms. But the idea of species as evolutionary groups
of species. But be sure to note the vagueness of these is in stark contrast to this categorical tradition that is
commonplace ideas of evolutionary groups. As much imbedded within our minds. The tradition of thinking of
as they are backed by strong theory, any attempt to species as evolutionary groups is only 140-years old, and
translate this theory into strict criteria for the it is knowledge that comes to a person late in life, at least
unequivocal identification of evolutionary groups compared with the knowledge of categories of organisms.
requires much work (and if the history of the species In short, we have two widely differing ways of
problem is any indication, is bound to fail). appreciating biological diversity17,21,33. We have the

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 Opinion TRENDS in Ecology & Evolution Vol.16 No.7 July 2001 329

ages-old instinct to categorize, and we have the modern different human observers will find different taxa. It is
tradition of scientific inquiry. Our instincts give us taxa, also useful to imagine a thought experiment of the taxa
but our inquires have only recently led us to understand that would be devised by an alien observer, by one who
evolutionary groups. The taxa are relatively easy to uses different senses and who operates on a different
find and invent, whereas the evolutionary groups are scale of observation.
difficult to study, for they are often truly indistinct (2) Real evolutionary groups need not be distinct, and
with fuzzy boundaries between groups, and the forces can overlap or be nested within one another, whereas
that conjoin them can be subtle. Research on a species, categories are created as a direct function of perceived
as an evolutionary group, requires study of the very distinction. Attempts to delimit evolutionary groups by
processes of direct and indirect interaction among the boundaries of the categories will cause some groups
organisms, including reproduction and competition, to be missed and others to be wrongly circumscribed.
that can cause those organisms to be a species. (3) Most importantly, we must keep in mind that the
evolutionary processes that caused the patterns that we
The causes of the species problem recognize, and which we use to form taxa, are processes
In addition to carrying conflicting ideas of species, we that acted long ago. As time passes, the wave front of
evolutionary biologists also try to do something else – evolutionary processes leaves behind strong patterns of
we try to find a way to have the taxa be the same as the similarity and differences among organisms. It is those
evolutionary groups. The two things are ontologically patterns that we use for the taxa, but the place where
different, but they can correspond when all those evolutionary groups exist is at that wave front – they are
organisms that we would place in a category also caused by the evolutionary processes that are going on
collectively and completely constitute an evolutionary right now. The patterns of similarity that we recognize
group. The human species is probably our most accessible are the remnants of former evolutionary groups that
example of a species taxon that also corresponds well to might have long since shifted and splintered.
an evolutionary group. In general, our taxa can serve as The species problem is caused by two conflicting
hypotheses of the organisms that constitute evolutionary motivations; the drive to devise and deploy categories,
groups. Evolutionary biologists are very familiar with and the more modern wish to recognize and understand
this mode of thought. However, we will fail in our studies evolutionary groups17. As understandable as it might be
if we forget the reasons why the two sorts of things that we try to equate these two, and as reasonable and
might have little correspondence with one another. correct as it might be to use taxa as starting hypotheses
(1) The patterns that we observe are a function of of evolutionary groups, the problem will endure as long
our own capacity for perception and judgment. as we continue to fail to recognize our taxa as inherently
Furthermore, there is no reason why our senses should subjective, and as long as we keep searching for a
be as subtle as all of nature. When we devise taxa, we magic bullet, a concept that somehow makes a taxon
are not objective, and we must keep in mind that and an evolutionary group both one and the same.
References pp. 28–59, Sinauer Associates University of Chicago Press
1 Mayr, E. (1982) The Growth of Biological Thought, 13 Cracraft, J. (1997) Species concepts in systematics 25 Berlin, B. (1992) Ethnobiological Classification,
Harvard University Press and conservation biology – an ornithological viewpoint. Princeton University Press
2 Stebbins, G.L. (1969) Comments on the search for a In Species: the Units of Biodiversity (Claridge, M.F. 26 Rosch, E. (1978) Principles of categorization. In
‘perfect system’. Taxon 18, 357–359 et al., eds), pp. 325–339, Chapman & Hall Cognition and Categorization (Rosch, E. and Lloyd,
3 Mayden, R.L. (1997) A hierarchy of species concepts: 14 Mayr, E. (1992) A local flora and the biological B.B., eds), pp. 28–48, Lawrence Arlbaum Associates
the denouement in the saga of the species problem. species concept. Am. J. Bot. 79, 222–238 27 Landesman, C. (1971) Introduction. In The Problem of
In Species: the Units of Biodiversity (Claridge, M.F. 15 Avise, J.C. and Wollenberg, K. (1997) Phylogenetics Universals (Landesman, C., ed.), pp. 3–17, Basic Books
et al., eds), pp. 381–424, Chapman & Hall and the origin of species. Proc. Natl. Acad. Sci. 28 Graham, M. (1996) Birds in double trouble. Nature
4 de Queiroz, K. (1999) The general lineage concept U. S. A. 94, 7748–7755 380, 666–667
of species and the defining properties of the species 16 Wheeler, Q.D. and Meier, R., eds (2000) Species 29 Zink, R.M. (1996) Bird species diversity. Nature
category. In Species (Wilson, R.A., ed.), pp. 49–89, Concepts and Phylogenetic Theory: a Debate, 381, 566
MIT Press Columbia University Press 30 Ghiselin, M.T. (1966) On psychologism in the logic
5 Keller, E.F. and Lloyd, E.A. (1992) Keywords in 17 Hey, J. Genes Categories and Species, Oxford of taxonomic controversies. Syst. Zool. 15, 207–215
Evolutionary Biology, Harvard University Press University Press (in press) 31 Ghiselin, M.T. (1987) Species concept, individuality,
6 Wilhite, D. and Glantz, M.R. (1987) Understanding 18 Popper, K.R. (1962) The Open Society and its and objectivity. Biol. Philos. 2, 127–143
the drought phenomenon: the role of definitions. Enemies, Routledge and Kegan Paul 32 Ghiselin, M.T. (1997) Metaphysics and the Origin
In Planning for Drought (Wilhite, D. et al., eds), 19 Levin, D.A. (1979) The nature of plant species. of Species, State University of New York Press
pp. 11–27, Westview Press Science 204, 381–384 33 Hull, D.L. (1976) Are species really individuals?
7 Dracup, J.A. et al. (1980) On the definition of 20 Endler, J.A. (1989) Conceptual and other problems Syst. Zool. 15, 174–191
droughts. Water Resour. Res. 16, 297–302 in speciation. In Speciation and its Consequences 34 Hull, D.L. (1978) A matter of individuality. Philos.
8 Caplan, A.L. et al., eds (1981) Concepts of Health (Otte, D. and Endler, J.A., eds), pp. 625–648, Sci. 45, 335–360
and Disease, Addison–Wesley Sinauer Associates 35 Hacking, I. (1983) Representing and Intervening:
9 Mayr, E. (1942) Systematics and the Origin of 21 Hull, D.L. (1997) The ideal species concept – and Introductory Topics in the Philosophy of Natural
Species, Columbia University Press why we cannot get it. In Species: the Units of Science, Cambridge University Press
10 Mayr, E. (1996) What is a species and what is not? Biodiversity (Claridge, M.F. et al., eds), pp. 357–380, 36 Dennett, D.C. (1991) Real patterns. J. Philos. 88,
Philos. Sci. 63, 262–277 Chapman & Hall 27–51
11 Cracraft, J. (1983) Species concepts and speciation 22 Heywood, V.H. (1998) The species concept as a 37 Haugeland, J. (1993) Pattern and being. In
analysis. Curr. Ornithol. 1, 159–187 socio-cultural phenomenon – a source of the Dennett and his Critics (Dahlbom, B., ed.),
12 Cracraft, J. (1989) Speciation and its ontology: the scientific dilemma. Theor. Biosci. 117, 203–212 pp. 53–69, Blackwell Science
empirical consequences of alternative species 23 Smith, E.E. and Medin, D.L. (1981) Categories and 38 Dobzhansky, T. (1950) Mendelian populations and
concepts for understanding patterns and Concepts, Harvard University Press their evolution. Am. Nat. 84, 401–418
processes of differentiation. In Speciation and its 24 Lakoff, G. (1987) Women, Fire, and Dangerous 39 Atran, S. (1990) Cognitive Foundations of Natural
Consequences (Otte, D. and Endler, J.A., eds), Things: What Categories Reveal About the Mind, History, Cambridge University Press

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 Review TRENDS in Ecology and Evolution Vol.18 No.11 November 2003 597

Understanding and confronting

species uncertainty in biology and
conservation
Jody Hey1, Robin S. Waples2, Michael L. Arnold3, Roger K. Butlin4 and Richard
G. Harrison5
1
Department of Genetics, Rutgers University, Piscataway, NJ 08854, USA
2
National Marine Fisheries Service, Northwest Fisheries Science Center, Seattle, WA 98112, USA
3
Department of Genetics, University of Georgia, Athens, GA 30602, USA
4
Centre for Biodiversity and Conservation, School of Biology, The University of Leeds, Leeds, UK LS2 9JT
5
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA

Recent essays on the species problem have emphasized species, but the problem endures with a steadily increas-
the commonality that many species concepts have with ing literature on how to define ‘species’. A recent listing of
basic evolutionary theory. Although true, such consen- species concepts found 24 in the modern literature [1] and
sus fails to address the nature of the ambiguity that is new books appear steadily [2 – 4].
associated with species-related research. We argue that In recent years, a recurring claim with regard to the
biologists who endure the species problem can benefit species problem is that most species concepts have strong
from a synthesis in which individual taxonomic species implicit similarities, and that most are consistent with the
are used as hypotheses of evolutionary entities. We dis- idea that species are evolving lineages or evolving
cuss two sources of species uncertainty: one that is a populations [1,3,5,6]. We agree with this consensus.
semantic confusion, and a second that is caused by the However, we remain concerned that it does little to
inherent uncertainty of evolutionary entities. The for- address the fundamental cause of the species problem,
mer can be dispelled with careful communication, which is the inherent ambiguity of species in nature. Here,
whereas the latter is a conventional scientific uncer- we focus directly on the nature of this ambiguity and
tainty that can only be mitigated by research. This review a modern synthesis under which species-related
scientific uncertainty cannot be ‘solved’ or stamped research and conservation efforts can proceed without
out, but neither need it be ignored or feared. suffering from, and without fear of, the ambiguity of
species.
For researchers, few ideals are as sought after as those of
the independent observer; preferably, a scientist should Background and synthesis
discover and transmit his or her story, and not be a part of Prominent in species debates are questions regarding the
it. But what if that cannot be arranged? In some fields, role played by human investigators in the creation of
most notably quantum physics and human behavioral species taxa, particularly with regard to taxonomic rank
research, observation per se can have a direct effect on
designations. Darwin argued that decisions to apply the
outcomes, so that studies must be designed to incorporate
taxonomic rank of species were sometimes arbitrary, and
those effects. Of course, research in these fields does not
that species are not different essentially from varieties [7].
come to a halt. Neither does research halt in other fields
Spurway drew upon the ways that animals learn to
where the impact of the observer cannot be avoided or
identify different kinds of organism to argue that species
ignored safely, but rather is addressed directly as part of
designations are caused by basic human instincts, and
the research program. Here, we argue that biological
that we could not expect to find a universally applicable
research on species will benefit from an explicit recog-
definition of ‘species’ [8]. Haldane supported this view [9],
nition of the inherent limitations that biologists experi-
ence as investigators of species. and it has been articulated more recently from different
Many evolutionary biologists, systematists and ecolo- directions by Levin [10] and Nelson [11]. Yet, these
gists struggle with the related questions of how to identify skeptics notwithstanding, the view has emerged since
species and how to define the word ‘species’. These Darwin that species have special properties that set them
persistent questions constitute what is known as the apart from taxa of other ranks, and that species are
‘species problem’. The problem is not new. Indeed, Darwin objective and real to some extent because of these
drew upon the persistence of wide taxonomic disagree- properties. Dobzhansky’s Genetics and the Origin of
ments to support his arguments for the evolution of Species portrayed species as real genetical and evolving
entities that could be studied with modern genetic
Corresponding author: Jody Hey (hey@biology.rutgers.edu). approaches [12]. Huxley’s The New Systematics [13] is
39
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598 Review TRENDS in Ecology and Evolution Vol.18 No.11 November 2003

the historical touchstone for modern systematic research might be simply confirmed or rejected, although more
programs that see species not just as categories with typical outcomes are likely to be fuller descriptions of the
representatives in museums, but also as dynamic evolving evolutionary processes that occur among the organisms
entities that exist independently of human observers and that would be identified as members of a taxon. Some
of human-assigned categories [14,15]. species taxa can be expected to be highly explanatory as
These two ideas – that species are categories that are evolutionary hypotheses, in which case they are likely to
created essentially by the biologists who study them, and be affirmed by the discovery of additional characters that
that species are objective, observable entities in nature – are shared uniquely among the organisms assigned to the
have long been in conflict. On the one hand, we have taxon. At some point following research on these evol-
species taxa that have been identified traditionally on the utionary processes, a taxon might come to be paired with a
basis of distinctive characteristics. On the other hand, we full description of the population or populations that it
have an idea of a species as a kind of entity in nature, an represents, including the degrees of isolation and distinc-
evolutionary unit made up of related organisms that are tion that occur among populations. Also, the degree or
evolving together. Over the years, various authors have quality of correspondence between a taxon and its evolving
recognized this fundamental distinction [3,16 –22]. Yet, is counterparts might be used to devise more taxa as
it possible that these two perspectives on species can be necessary.
joined? That has been the intended purpose of some
popular species concepts, and much of the modern debate The ambiguity of species entities
over species concepts has been a struggle over how best to From a purely ontological perspective, entities are real
describe species in a way that preserves both the accepted things that have a location in space and time, and that can
taxonomic traditions and the modern understanding of be acted upon or can change [36]. Entities have a different
evolutionary processes. Both the Biological Species Con- kind of existence than do categories, such as taxa, which
cept of Mayr [23,24] and the Phylogenetic Species Concept have defining properties. To be clear, by way of a deliberate
of Cracraft [25,26] are intended to help biologists identify example, consider the species taxon Ursus maritimus
species taxa that are real evolutionary role players in (polar bear). The defining properties of this taxon were
nature. Neither view admits a distinction between species described first by Constantine Phipps [37]. Today, many
taxa and species as evolutionary entities. animals that we assign to this taxon live in zoos, but most
But, hidden partly in the debates over the nature of constitute a circumpolar arctic population, comprising
species lies a direct and complementary connection multiple connected regional populations; that is, an
between species as taxa and species as entities. The evolving entity [38]. Even if this entity were to disappear,
connection represents a conceptual linkage that circum- and the natural population of polar bears were to become
vents many aspects of the species problem and that leads extinct, the species taxon would still exist as a set of
directly to ways that research can proceed without species defining characteristics and would still have representa-
conflicts. To see this connection, consider that newly tives in museums or zoos.
devised species taxa serve as hypotheses that might be Species are but one kind of multi-organismal entity, and
supported by new data and that, notwithstanding the rule organisms can also be components of social groups within
of precedence, might require later revision. Growing species as well as parts of commensal interspecies
collections, improving methods of morphological analysis, assemblages. Biologists also recognize ecological entities
and the increasing use of ecological, behavioral and genetic that consist of many different kinds of organisms, and
data have moved biologists necessarily away from the view individual organisms are parts of ecosystems, both on very
of taxa as fundamentally static to a view in which species local and broad scales. To complete the point, we need not
taxa can be revised on the basis of increasing information be monistic with regard to species entities and so might
from diverse sources [13– 15,27,28]. This view, that our wish to consider different kinds of species entities as a
ideas regarding a particular species should be subject to function of how they arise and persist. Templeton [39]
examination in light of data from natural populations, has articulated two general processes that will cause a group of
also emerged in the population genetic literature [29,30]. organisms to evolve together: gene exchange and ecologi-
In particular, Templeton argues that population genetic cal equivalence (or demographic exchangeability). Both
data should be used to test whether populations do indeed processes, alone or together, can cause genetic drift and
exist as cohesive species [31]. adaptations to be shared by a group of organisms, and
These twin strands of thought on the hypothesis-testing cause that group to evolve cohesively and separately from
aspect of species designations, from the perspectives of other such groups.
both systematics and population genetics, lead to the idea Our perceptions of an evolving group of organisms will
that a species taxon can serve as a hypothesis of a species be least ambiguous for those taxa whose only representa-
as an evolutionary and ecological unit in nature [3,32– 35]. tives exist in a single, small distinct population (e.g. a
This synthesis draws directly upon the practice in species restricted to a single lake or mountain peak). But
systematics in which taxa are subject to revision, but, in even small populations that appear cohesive and well
addition, there is the idea that a species taxon presents a bounded in some respects might not be in others. The
general hypothesis that all existing organisms that would population of finches of the species taxon Geospiza fortis
be assigned to that taxon actually constitute a biological that lives on Isla Daphne Major in the Galapagos is not
entity in nature. separated completely from populations on other islands,
In principle, species taxa that are used as hypotheses neither is it completely separate from populations that are
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 Review TRENDS in Ecology and Evolution Vol.18 No.11 November 2003 599

assigned to other taxa [40,41]. Episodic hybridization Type II uncertainty

results in gene flow, and introgressing traits from other The second kind of uncertainty arises from basic limi-
species are sometimes favored by natural selection. In this tations of empirical scientific research. This uncertainty is
case, detailed genetic and ecological data reveal both the caused by the inherently ambiguous correspondence
presence of a cohesive evolving population, as well as ways between a species taxon and the entity or entities for
in which that population is not entirely separate from which it is used as a hypothesis. Even with clarity over the
other populations, some of which are assigned to the same distinction between a taxon and an evolutionary entity, it
taxon and others to different taxa. might be very difficult to assess empirically the actual
We might expect that large populations, especially if correspondence for a particular taxon. This practical,
they are subdivided geographically, will often comprise empirical uncertainty is conventional in the sense that
multiple evolutionary entities. A taxon might include scientists are rarely fully assured of a correspondence
organisms that are found in isolated populations, each of between their hypothesis and reality. At base, this
which is evolving separately. Such populations might be uncertainty arises because of the subjective component
connected tenuously by occasional gene flow, and thus of devising categories. Species taxa are devised by
might share some common selective sweeps (i.e. fixations investigators and are partly a function of biologists’
of advantageous mutations) and adaptations [42], but they tools, circumstances and inclinations. For species that
might still occur mostly as separate populations. In these can be observed easily and have distinguishing morpho-
contexts, the nature of the evolutionary entity could be logical characters, this subjective element will seem
inherently ambiguous, and even intensive field research remote and biologists can agree on the organisms to be
will not reveal a clear demarcation. In short, all the included in a species taxon. However, for many organisms
organisms of a species taxon will often not constitute an that live in soil or water, or within or upon other larger
evolutionarily cohesive entity, particularly for species taxa organisms, the subjective element might be large. Two
with representatives that are widespread or have disjunct investigators working with a common sample of organisms
distributions [43]. might well disagree on the weight to be given to particular
patterns of variation in such cases, and thus on the
designations and descriptions of new species taxa. When
Understanding species uncertainty we turn to the field, and use species taxa as hypotheses, we
Using species taxa as a framework to study evolving see also that the uncertainty is difficult to mitigate. In
species in nature reveals two different kinds of uncertainty short, species entities are very difficult to study, for they
that might persist in species-related research and are evolutionarily and demographically dynamic. They
discussions. will often not be very distinct and the degree to which they
are distinct can change over time [5] if, for example,
separated populations exchange genes occasionally (as is
Type I uncertainty the case with the Galapagos finches).
One persistent component of the species problem is that
‘species’ is a confusing homonym, with different meanings Confronting species uncertainty
that are disparate ontologically and yet related semanti- Across the breadth of species-related research, biologists
cally. Three ontologically distinct meanings predominate vary in their use of species taxa. In systematics, taxa are
in the literature of the species problem: (1) ‘species’ is the the essential starting point for classification and phyloge-
name of a taxonomic rank; (2) ‘species’ is the word that we netic research. In population biology, some taxa are also
apply to a particular taxon of that rank (e.g. the species used in the course of ecological or genetic research on the
taxon Homo sapiens); and, finally, (3) ‘species’ is a word structure of evolving populations, although only a few can
that we apply to an evolving group of organisms. The be examined in this way. In the continuum of research
potential for confusion between the first two meanings, the programs, which lies between focused taxonomic research
taxonomic rank and particular taxa, has been recognized on the one hand, and research that is focused on particular
for some time [18,44,45]. Less widely realized is that populations in nature on the other, there lies a great deal of
confusion also arises between the second and third research by ecologists, evolutionary biologists and con-
meanings, between the ideas of a species as a taxon servation biologists that rely upon taxa as indicators of
(i.e. a category of organism or a group of organisms with a evolutionary entities. For example, many multi-species
shared set of traits) and a species as an evolving group of studies, including ecosystem studies and biodiversity
closely related organisms. Although biologists and philo- assessments, rely strongly upon species taxon counts.
sophers have recognized that evolution creates entities Such counts suffer several limitations depending on the
that comprise multiple related individuals [23,36,46,47] it context, but one that is typically overlooked is the usually
has been understood only at times that such things are not unknown correspondence between taxa and evolutionary
literally the same things as taxa (i.e. kinds of organisms) entities [22,48,49].
[3,16,17,34]. That one word, ‘species’, is sometimes What do we gain by considering species taxa explicitly
used to refer to a taxonomic rank, at other times a as hypotheses of species entities in nature, and by dividing
particular taxon, and at other times an entity in our species-related uncertainty into semantic (type I) and
nature, causes confusion and requires that authors and empirical (type II) components? For research on natural
speakers take care to articulate their meaning when populations, for evolutionary and ecological questions or
they use the term. for efforts to conserve biological diversity, we gain a
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600 Review TRENDS in Ecology and Evolution Vol.18 No.11 November 2003

general research protocol that is not hindered by some of The common assertions, that we must be able to both count
the traditional species-problem debates. Of course, the species and to distinguish species, are directly answerable:
method is not thereby made easy or simple. No synthesis (1) species taxa can be counted, and they are distinguished
can do that because species in nature are difficult subjects. in the course of their devising; whereas, (2) evolutionary
However, we can appreciate that the difficulty of studying entities will often be truly indistinct, and will sometimes
species is a conventional scientific difficulty; it is caused by not be countable strictly or distinguishable unambigu-
the need to devise and test hypotheses, just as in other ously no matter how thoroughly they are studied [34].
fields with difficult subjects.
The framework of treating species taxa as hypotheses of Identifying units for conservation
species entities leads us to distinguish those aspects of The contrast between species taxa and evolutionary
species uncertainty that are inherent to research and entities is stark when considering conservation. Species
discovery of biological diversity, and to set aside some taxa can often be preserved in the sense of having living
aspects of species-related debate that are avoidable. Two representatives by culturing organisms in zoos and
basic questions are inescapable. First, by what criteria botanical gardens; that is, by maintaining living counter-
shall species taxa be identified? For systematists, this parts to the taxon representatives that are kept in
question lies at the heart of species-concept debates museums. But if species taxa are to have representatives
[2,15,50,51]. However, when a taxon is to be a tool for the living in nature, then they must be part of evolving
study of evolutionary entities, then the question becomes populations. In recent decades, this simple realization of
the following: what criterion will aid best in the discovery the fundamental insufficiency of taxa as the focus of
of the locations, boundaries and properties of evolutionary conservation efforts has shifted those efforts towards
entities? Importantly, the answer might not be the same research on how best to conserve evolving populations [54].
for all kinds of organisms. For population-based conservation efforts to be effec-
The second question is when does one decide that there tive, goals must be articulated clearly both in terms of
is one, or more than one, evolving entity? Two kinds of what kinds of populations are to be conserved and in terms
answer come fairly readily. One is simply not to decide that recognize the inherent difficulties and ambiguities. To
whether or where to draw lines of demarcation, but rather appreciate how such apparently offsetting demands (for
to present the full picture that research has revealed, and conservation criteria that recognize inherent ambiguities)
to do so in its full complexity rather than to reduce that can be implemented, and to appreciate the issues raised by
complexity artificially. A second kind of resolution, which their application, we consider the entity-based idea of an
might be demanded because of practical concerns, is to evolutionary significant unit (ESU) [55– 58]. An ESU is a
make a decision regarding demarcations, while also population, or group of closely connected populations, that
recognizing the decision as an oversimplification belong to a species taxon. Furthermore, an ESU shows
demanded by the practical concerns. evidence of being genetically separate from other
The principal aspect of the species problem that is populations, and contributes substantially to the
avoided by our proposed synthesis is the traditional debate ecological or genetic diversity found within the species
over a ‘best’ species concept. Consider that if taxa are to taxon as a whole.
serve as hypotheses, then there are several common In recent years, the ESU concept has been applied
species concepts and associated taxonomic criteria that broadly to salmon populations on the west coast of the
could provide a good starting point for the study of USA, as well as to a variety of other species [58,59]. The
populations. In particular, the use of reproductive traits intent in defining salmon ESUs has been to identify
and the use of diagnostic characters are both well entities that are on largely independent evolutionary
motivated by evolutionary theory, and each is expected trajectories. Although it is problematic to predict which
to provide a rough guide to the presence of evolutionary ESUs will be important to the future evolution of the
units in nature [6]. This is not to say that one is as good as taxon, conservation of as many ESUs as possible should
another in a particular context, simply that each is minimize anthropogenic constraints on natural evolution-
justifiable in principle, and that it remains to inves- ary processes and maximize the probability that the taxon
tigators to make that justification for their particular and some of its populations will persist into the future.
subjects of research. However, this formulation provides no specific, quantitat-
A key inspiration of the species-concept debate is the ive standards and offers no guarantees that type II
often-described need for species-related clarity. These uncertainties will be resolved. Thus, several variations
appeals say in part that we need a common concept of of the ESU concept have been proposed, and the concept
species to handle the uncertainties that arise in species- has been criticized as being too broad [60], too narrow
related research. Although true in strictly systematic [61,62] or non-operational [52,63]. Two different kinds of
contexts, the same arguments have also been applied in approach have been suggested to address the apparent
reference to the study of evolving populations in nature vagueness of the ESU concept. One suggestion is that, for
[26,52,53]. However, no species concept or protocol can the purposes of efficiency, ESU status should be decided
remove the inherent difficulty and ambiguity of research using a uniform standard of genetic cohesiveness and
on evolving populations. The demarcation of two different uniqueness. For example, Moritz [60] suggested a specific
sources of species uncertainty leads to a fairly straightfor- genetic cutoff (based on mitochondrial DNA monophyly
ward parsing of conventional demands for species-related and nuclear gene differences) for conferring ESU status.
clarity into those that are tractable and those that are not. The obvious concern that application of that standard will
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 Review TRENDS in Ecology and Evolution Vol.18 No.11 November 2003 601

appear arbitrary in many applications, or capricious in the taxa as a strategy to serve conservation goals, or to shift
face of other kinds of evidence of cohesiveness and the rank of a taxon solely as a way to preserve biodiversity
uniqueness is perhaps answered by the considerable [71]. In other words, legitimate conservation concerns,
need for a readily applicable, if imperfect, yardstick. combined with a reliance on taxa as conservation units,
Given that mitochondrial DNA diversity will often be a can have the unfortunate consequence of shifting taxo-
poor indicator of demographic boundaries [64– 66], this nomic decisions away from biological criteria and towards
particular proposal might not be ideal. However, this does political or economic concerns.
not mean that some standardized method might not Second, the uncertainty of species entities is not
provide a reasonable balance between biological realism different in kind to that associated with other scientific
and the needs for efficiency. subjects. Importantly, many scientific pursuits have high
A different kind of suggestion is that the current ESU levels of uncertainty and also play a highly visible role in
criteria should be replaced by a single, better criterion that the formation of public policy. Consider droughts, for
would, inherently by its nature, dispel uncertainty. The example, which, as phenomena, are not circumscribed
principal claim of this sort is that ESUs should be groups easily, their intense environmental and financial impact
of individuals that share a unique character, or suite of notwithstanding. Meteorologists, hydrologists and policy
characters, that distinguish them from individuals of planners have worked to develop practical guidelines for
other ESUs [52,63]. In other words, an ESU should be drought identification, even as they debate how best to do
identified by the criteria used in one version of the so [72]. Consider as well the difficulties associated with
Phylogenetic Species Concept [67,68], not for reasons of medical diagnosis and the identification of health-risk
efficiency (which could also be claimed), but because such factors. Physicians must make judgment calls regularly in
criteria are inherently unambiguous indicators of real the care of their patients, and they must also provide
evolutionary entities. These proposals, which equate the public health guidelines that are as unambiguous as
presence of a disjunct pattern of characters with the possible, often in the face of substantial inherent
presence of an evolving population, have two limitations. ambiguity.
First, they assume accuracy on the part of taxonomic The question of how best to identify populations for
criteria and overlook the reasons why species taxa will conservation has much in common with questions of how
often be a poor guide for elucidating evolutionary entities. to identify droughts, and to prevent or treat disease, and
Second, by directly equating ESUs with species taxa they with other areas where imperfect scientific knowledge is
have nothing to offer to the question of how best to used to shape public policy. The choices of what to conserve
conserve diversity below the species level. must often be made with regard to populations that are not
In the case of Pacific salmon, the recognized species separate completely from others, or when information
taxa that are based on diagnostic characters are consider- regarding the relationships and degrees of distinction
ably more inclusive than ESUs that have been identified, among populations is very incomplete. Such decisions,
each of which is limited to the populations in a restricted although difficult because of the uncertainties that are not
geographic area [58]. For this species, taxa based on mitigated easily, are not different in kind from those
diagnostic characters appear to be too coarse a guide for decisions made in other contexts where scientists have
identifying evolutionary entities, which is not surprising imperfect knowledge or where nature does not present
given the highly structured populations of anadromous clear boundaries.
fish. In other contexts, it might happen that a strong focus
on diagnostic characters could lead to taxa that are less Prospects
inclusive than true evolutionary entities, either because of Biologists cannot hope to avoid or eradicate species
the vagaries of sampling or because of the near infinity of uncertainty. Whether such hope arises from a wish to
possible characters to examine [69]. ‘solve’ the species problem, or from a wish to simplify the
tasks of biodiversity conservation, or from fear that policy-
Policy implications of species uncertainty making and legal institutions cannot accommodate uncer-
If conservation efforts do focus on evolving populations and tainty about species, we should recognize that there is not
treat species taxa as research guides, then the ambiguity a single species concept, nor a research protocol, that can
of evolving populations and their uncertain connection to remove the inherent difficulty and uncertainty that
taxa will often be manifest. If biologists making conserva- accompanies research on evolving populations. These are
tion recommendations are revealed as being uncertain in conventional scientific uncertainties, and we cannot
their species assessments, will this hinder the legal and shelter ourselves from them.
policy-making components of species conservation? Per- The first reward of treating species taxa as hypotheses
haps if biologists admitted uncertainty over species, then and by recognizing the inherent uncertainties of species-
they could not play as constructive a role in conservation related research is a research protocol that is convention-
efforts [70]. For two reasons, we think that such a concern ally hypothetico-deductive. But beyond this aspect, which
is misplaced. already characterizes the work of many investigators, the
First, the traditional practice of treating species taxa as largest gains will be in the area of explanation. Research-
the primary focus of conservation efforts has a cost, quite ers of biological diversity are sometimes entangled by
apart from that associated with the possible misidentifica- species-problem-related questions that come from col-
tion of evolving populations. A strong reliance on taxa as leagues and biologists in other specialties, as well as from
conservation units creates a pressure to devise new species laypersons, students and professionals in fields who rely
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602 Review TRENDS in Ecology and Evolution Vol.18 No.11 November 2003

upon the conservation recommendations of biologists. By Consequences (Otte, D. and Endler, J.A., eds), pp. 28 –59, Sinauer
explaining how research begins with taxa and proceeds to Associates
26 Cracraft, J. (1997) Species concepts in systematics and conservation
the study of populations, many species puzzles can be biology – an ornithological viewpoint. In Species: the Units of
explained in the familiar language of the uncertain Biodiversity (Claridge, M.F. et al., eds), pp. 325 – 339, Chapman & Hall
relationship between our hypotheses and the realities of 27 Constance, L. (1951) The versatile taxonomist. Brittonia 7, 225 –231
nature. 28 Ertter, B. (2000) Floristic surprises in North America north of Mexico.
Ann. Miss. Bot. Gard. 87, 81 – 109
29 Sites, J.W. and Crandall, K.A. (1997) Testing species boundaries in
Acknowledgements
biodiversity studies. Conserv. Biol. 11, 1289 – 1297
We are grateful to three reviewers for very helpful comments and to John
30 Templeton, A.R. (1994) The role of molecular genetics in speciation
Avise for input on the article. Jim Mallet provided valuable input
studies. In Molecular Approaches to Ecology and Evolution (Schier-
throughout much of the preparation of the paper, although he disagrees
water, B. et al., eds), pp. 455 – 477, Birkhäuser-Verlag
with some important aspects. M.L.A. acknowledges support from the
31 Templeton, A.R. (2001) Using phylogeographic analyses of gene trees
National Science Foundation, grant DEB-0074159.
to test species status and processes. Mol. Ecol. 10, 779 –791
32 Baum, D.A. and Donoghue, M.J. (1995) Choosing among alternative
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Endeavour
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The history of reductionism versus holistic approaches to scientific research by H. Andersen
Reading and writing the Book of Nature: Jan Swammerdam (1637–1680) by M. Cobb
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The role of museums in history of science, technology and medicine by L. Taub
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Who Needs Sex (or Males) Anyway?
Liza Gross | doi:10.1371/journal.pbio.0050099

If you own a birdbath, chances are

you’re hosting one of evolutionary
biology’s most puzzling enigmas:
bdelloid rotifers. These microscopic
invertebrates—widely distributed
in mosses, creeks, ponds, and other
freshwater repositories—abandoned
sex perhaps 100 million years ago, yet
have apparently diverged into nearly
400 species. Bdelloids (the “b” is silent)
reproduce through parthenogenesis,
which generates offspring with
essentially the same genome as
their mother from unfertilized eggs.
Biologists have yet to find males,
hermaphrodites, or any trace of
meiosis—the process that creates
sex cells—challenging the long-held
assumption that evolutionary success
requires genetic exchange.
The genetic variation created by
meiosis and fertilization, theory holds,
bolsters a species’s capacity to weather
shifting environmental conditions
or resist rapidly evolving parasites.
(During meiosis, the genome splits
in two, and chromosome pairs swap
bits of their DNA; during fertilization,
the sex cells fuse to restore the
complete genome.) Many multicellular
eukaryotes pass through a sexual and
asexual phase in their life cycle. But
doi:10.1371/journal.pbio.0050099.g001
eschewing sex altogether, à la bdelloids,
is not theoretically consistent with a Scanning electron micrographs showing morphological variation of bdelloid rotifers and
long-lived evolutionary life span or their jaws. Have these asexual animals really diversified into evolutionary species? (Image:
extensive species diversification. Diego Fontaneto)
In a new study, Diego Fontaneto,
Timothy Barraclough, and colleagues species, but it can’t distinguish species cohesion and divergence, then
developed new statistical techniques whether such differences reflect asexual taxa should diverge along the
for combined molecular and physical variations among a same lines as sexually reproducing
morphological analyses of rotifers group of clones or adaptations organisms. And if this were the case,
to test the notion that species among independently evolving they would expect to find genetic
diversification requires sex. The populations. In the traditional and morphological cohesion within
researchers show that, despite an view of species diversification, independently evolving populations
ancient aversion for interbreeding, interbreeding promotes cohesion and divergence between them.
bdelloids display evolutionary patterns within a population—maintaining the To detect independently evolving
similar to those seen in sexually species—and barriers to interbreeding populations, the researchers analyzed
reproducing taxa. How they have (called reproduction isolation) marker genes isolated from clones
avoided the pitfalls of a lifestyle widely promote species divergence. With no of bdelloids collected from diverse
regarded as evolutionary suicide interbreeding to maintain cohesion, habitats around the world. They
remains an open question. the thinking goes, asexual taxa might constructed evolutionary trees using
Bdelloids have remained such an not diversify into distinct species. both mitochondrial and nuclear
enduring enigma in part because Fontaneto et al. defined species DNA sequences (the molecular
biologists are still debating whether as independently evolving, distinct “barcode” cox1 and 28S ribosomal DNA
species exist as true evolutionary populations (or units of diversity) sequences, respectively) to identify
entities. And if they do, what forces subject to distinct evolutionary species within the samples. For the
determine how they diverge? mechanisms. They predicted that if morphological analysis, they measured
Traditional taxonomy relies on factors other than interbreeding—such the size and shape of the rotifers’ jaws
morphological differences to classify as niche specialization—controlled (called trophi).

PLoS Biology | www.plosbiology.org 46

0001 April 2007 | Volume 5 | Issue 4 | e99
 The morphological results largely researchers show that these distinct Altogether, these results show that
fell in line with traditional taxonomic monophyletic genetic clusters the asexual bdelloids have indeed
classifications for most bdelloid represent independently evolving experienced divergent selection on
species. And species identified as entities (rather than variations within feeding morphology, most likely as
related on the DNA trees typically a single asexual population). But what they adapted to different food sources
had similar morphology. The caused them to evolve independently? found in different niches. By showing
correspondence between the molecular Are they geographically isolated that asexual organisms have diverged
and morphological results suggests populations that evolved under neutral into “independently evolving and
that the majority of traditionally selection, or did they evolve into distinct entities,” the researchers argue,
identified bdelloid species are what’s ecologically discrete species as a result this study “refutes the idea that sex
known as monophyletic—individuals of divergent selection pressures on is necessary for diversification into
in the same species assort together trophi morphology? evolutionary species.” They hope others
on the evolutionary tree and share a If bdelloids have experienced use their approach to study mechanisms
common ancestor. Only two of these divergent selection, the researchers underlying species divergence in sexual
traditional, monophyletic species explain, they would expect to see taxa to clarify the hazy nature of species
showed significant variation in trophi high variation in trophi traits between and biological diversity.
size or shape among the populations; species, and low intraspecies variation
both also showed significant divergence (compared to neutral changes). And Fontaneto D, Herniou EA, Boschetti
in the DNA trees. that’s what they found—bdelloids have C, Caprioli M, Melone G, et al. (2007)
Using statistical models to determine experienced divergent selection on Independently evolving species in asexual
the likely origin of the observed trophi size (and to a lesser degree, on bdelloid rotifers. doi:10.1371/journal.
DNA tree branching patterns, the trophi shape) at the species level. pbio.0050087

PLoS Biology | www.plosbiology.org 47

0002 April 2007 | Volume 5 | Issue 4 | e99
Reviews

Santa Rosalia Revisited:

or Why Are There So Many Kinds of Parasites in
‘The Garden of Earthly Delights’?*
T. de Meeûs, Y. Michalakis and F. Renaud

As is the case for free-living species, a very large number of Limitations of the BSC for parasites
parasitic species are not described adequately by the biological Parasitic organisms constitute a large proportion of
species concept. Furthermore, Thierry de Meeûs, Yannis the cases problematical to the BSC. Many parasite taxa
Michalakis and François Renaud argue that because hosts exhibit extremely restricted cross fertilization. Such
represent a highly heterogeneous and changing environment restrictions may be due to extreme rates of clonal
as well as a breeding site, favouring the association of host- reproduction, selfing or biparental inbreeding such as
adaptation and host-choice genes, sympatric speciation may sib-mating. Parthenogenesis is very well documented
occur frequently in parasitic organisms. Therefore, parasites in numerous families of nematodes parasitic on plants
appear to be ideal biological models for the study of ecological and animals12. The large controversy concerning the
specialization and speciation. Beyond the relevance of such clonality of many microparasites illustrates clearly the
considerations in fundamental science, the study of the origin opposition between parasites and the BSC13–15. The
and evolution of parasite diversity has important implications most spectacular examples of selfing lie within the
for more applied fields such as epidemiology and diagnosis. cestode group. Taenia solium, which is nearly always
found alone in the human intestine, can only self-
The biological species concept (BSC) which emphasizes reproduce16. In the Cyclorchida genus, because of ana-
the role of reproductive isolation1 remains widely used tomical constraints of the genitalia, self-fertilization is
despite the fact that it cannot account satisfactorily for a the only possibility16. Sib-mating is also often encoun-
large number of biological examples2. Furthermore, be- tered among parasites. For instance, in many hymen-
cause it focuses on the outcome and not the process, it opteran parasitoid wasps, such as Nasonia vitripennis,
has been detrimental to studies on mechanisms of speci- mating occurs only between brothers and sisters17.
ation3 and, in particular, it has served as a background Finally, many species undergo phases of asexual
to the main arguments against the existence of sympat- reproduction and sib-mating. For example, in many
ric speciation. Santa Rosalia was first mentioned by helminths the intermediate host is infected only by one
Hutchinson4 to provide a functional explanation for the individual, which undergoes asexual multiplication.
origin and apportionment of animal species. Several The products of this asexual multiplication in the inter-
authors subsequently referred to him in order to discuss mediate host are likely to mate together in the defini-
the existence of non-allopatric modes of speciation5,6. tive host. Such a mating system, genetically synony-
As mentioned previously by Lymbery7,8, for some mous with selfing, occurs in cestodes8 and trematodes18.
parasites the BSC has many limitations. Indeed, it fo- Applying the BSC to any of the previous examples
cuses on reproductive isolation as the unique criterion to would lead us to consider each individual as a single
delimit the species boundaries. Thus, the BSC confuses species and each egg hatching as a speciation event.
one consequence and its cause: reproductive isolation ‘Too much’ sex, however, is also encountered in
and the processes leading to it3. Given these limitations, parasites. The most well-known example concerns
several alternatives to the BSC have been proposed2,3,8. the genus Schistosoma, where hybridizations have
Many examples illustrate the inadequacy of the been described between different species19,20. This is
BSC. Indeed, large parts of the living world lie out- also known to occur between Echinostoma species21.
side the BSC’s logical domain, because they display Furthermore, bacteria can exchange DNA even be-
either ‘too little’ or ‘too much’ sex3. Obviously, the BSC tween distant ‘species’22,23. Hybridization itself may
is applicable only to sexually reproducing organisms9. also lead to speciation through polyploidization in
Moreover, self-mating and sib-mating organisms and parasites as, for example, in Paragoni-mus flukes24,
any other closed system of mating cannot be ac- thus fully contradicting the BSC. This process is
counted for satisfactorily by the BSC. In addition, probably largely overlooked in parasites and the few
many species are able to hybridize with others with- examples available concern human parasites.
out losing their ecological and genetic identities
through time3,10. Paradoxically, in some cases it is the Sympatric speciation in parasites
hybridization itself that leads to new species. Indeed, All these examples illustrate the fact that the BSC
many polyploid lineages are known to result from a cannot be applied to a large number of parasite
hybridization event between two different species11. species. These considerations are, arguably, only
semantic, requiring a solution only for the excep-
tions. However, BSC, by definition, brings problems
Thierry de Meeûs and François Renaud are at the Laboratoire
de Parasitologie Comparée, UMR 5555 CNRS, Université Montpellier of another order: it may lead to the mechanisms
II, Place E. Bataillon, 34095 Montpellier Cedex 05, France. Yannis * ‘The Garden of Earthly Delights’ refers to the triptych by Hieronymus
Michalakis is at the Laboratoire d’Ecologie URA 258, Université Bosch (c. 1500; Museo del Prado, Madrid) and, particularly, to its right panel
Paris 6 CC 237, 7 quai Saint Bernard, Bât. A, 75252 Paris Cedex 05, which exhibits an impressive collection of tormenting creatures that a biolo-
France. Tel: +33 4 67 14 37 09, Fax: +33 4 67 14 46 46, gist could recognize as the likely outcomes of recombination, hybridization
e-mail: renaud@crit.univ-montp2.fr and mutation combined with diversification.

10 48
Copyright © 1998, Elsevier Science Ltd All rights reserved 0169–4758/98/$19.00 PII: S0169-4758(97)01163-0 Parasitology Today, vol. 14, no. 1, 1998
 Reviews
responsible for reproductive isolation being over-
Box 1. Concepts of Allopatry and Sympatry in
looked3. Indeed, even if many sexually reproducing Parasitic Organisms
species can be recognized through the BSC, one can
consider that the reproductive isolation they display
against other species originated from other processes,
independent of those that led to such an isolation.
Thus, any evidence of reproductive isolation between
two closely related species provides no information on
the processes responsible for such an outcome. The
real problem here is less to testify the existence of
reproductive isolation than to understand the under-
lying mechanisms. When speciation is allopatric, repro-
ductive isolation is coincidental: while the different gene
pools are allopatric, selection will not act in favour of
isolating mechanisms. Characters diverge between gene
pools either by chance, or to adapt to different environ-
ments or genomic composition. Reproductive isolation
on secondary contact may arise only coincidentally to
this divergence. Selection for such isolating mechanisms
comes into action only after secondary contact, ie. when
different genetic entities are sympatric.
Under the BSC, the factors responsible for repro-
ductive isolation in general play no direct role in
species divergence3; therefore, all theoretical attempts
using the BSC as a basis have failed to describe sym-
patric speciation as a probable event5,25. Indeed, the
evolution of reproductive isolation per se is unlikely Different entities will be allopatric only if isolated geo-
because it will behave as a deleterious character when graphically. Individuals belonging to allopatric groups
rare, ie. in any case at the initial stage of the process. cannot interact. This is the case when different parasite
Alternatively, sympatric speciation may occur with- species live on different host species in areas where hosts
out the need to invoke reproductive isolation, through are separated by physical barriers (a; solid lines), or in
adaptive polymorphism and habitat preference26. As areas where vicariant host species replace one another
without any obvious physical barriers (b). On the con-
a recent study shows27, the result of these mechanisms trary, when encountered in the same geographical areas,
may be reinforced by any non-habitat-associated such entities will be considered sympatric, even if ex-
assortative mating. This process has been supported ploiting different resources. Indeed, in such co-existing
by some experimental work28 but the most convincing groups, individuals may still interact during their life
evidence is provided by the natural example of the cycle. For example, all helminths parasitizing the verte-
phytophagous insect Rhagoletis pomonella29 – a parasite. brates living in a pond are sympatric, because of all the
Because parasites provide particular situations, existing ecological interconnections between the hosts
Box 1 illustrates the difference between true allopatric and their parasites (c). More spectacular sympatric cases
and true sympatric situations found in host–parasite arise when parasites specialize on different organs of the
systems. Allopatric speciation alone can hardly ac- same host species (d). G, geographical areas; H, host
species (triangles), partitioned into different organs (inter-
count for the diversity of unambiguous species of nal triangles); closed circles represent parasites.
related parasites often encountered in a single host
(Fig. 1). Considering the parasitological literature this
situation is far from marginal. Among the platy- by at least seven species of mallophagous insects,
helminths, the monogeneans and cestoda provide each of which is specialized on a single feather type31.
the most striking examples. In the Tchad Basin (West Less spectacular in diversity, but necessarily recent, is
Africa) the characid fish Alestes nurse is known to the case of the three species of human lice32.
harbour on its gills eight monogenean species of the Furthermore, the most relevant evidence of on-
Anulotrema genus, each of which displays specific going sympatric divergences comes from the parasito-
genitalia (Fig. 1). These parasites, as well as their host, logical literature. In the Caribbean, the acquisition of
live only in this area so that their divergence and a murine host by the human parasite Schistosoma
speciation probably occurred in sympatry. In the mansoni leads to an adaptive divergence depending on
Mediterranean, the gills of the fish Liza saliens the periodic behaviour of the host towards water33.
(Mugilidae) are parasitized by four species of Ligo- The sea louse Lepeophtheirus europaensis also displays
phorus. In both cases, different parasite species are a sympatric divergence between the two flatfishes it
distributed non-randomly on different parts of the parasitizes in the Mediterranean (brill and flounder) –
gills (Fig. 1). Niche differentiation and specialization a supposedly recent phenomenon34. However, the
most likely led to speciation of these parasites on the better-documented studies come from insect parasites
same host species in a single geographical area. Among of plants35–38. Among these, Rhagoletis pomonella rep-
the Cestoda, four species of Acanthobothrium are de- resents a well-studied model29,39.
scribed in the spiral valve of the stingray Dasyatus When one considers the realm of microparasites,
longus from the Gulf of Nicoya (Costa Rica)30. reproductive isolation appears irrelevant as a mecha-
Other examples can be found among terrestrial nism for discriminating species. The tremendous
arthropods (lice). The bird Ibis falcinellus is parasitized diversity observed in groups such as the yeast Candida
Parasitology Today, vol. 14, no. 1, 1998 49 11
Reviews
factor is supported by comparative
analyses of herbivorous insects. Phy-
tophagy is encountered in only nine
of the 13 orders of insects44, but
these orders account for approxi-
mately half of all insect species.
Furthermore, phytophagous taxo-
nomic groups are significantly more
speciose than homologous groups
of the same evolutionary age with
a non-parasitic feeding habit44. A
possible explanation for this di-
versifying role of parasitism may
lie in the fact that sympatric speci-
ation is much more likely in
parasitic species. Indeed, as stated
previously, hosts provide ample
opportunities for niche diversific-
ation among parasite populations,
a necessary condition for sym-
patric speciation. Thus, sympatric
speciation may play a much more
central role in parasite evolution
and evolutionary biology as a whole,
with parasites representing ideal
biological models for the study
of ecological specialization and
speciation mechanisms.
Fig. 1. Two relevant examples of multiple monogenean congeners found in one host In the face of this acute potential
species and for which allopatric speciation alone cannot explain the observed diver- for diversification, hosts have
sity16. Morphology of male and female genitalia of eight species of Annulotrema failed to eliminate all their para-
observed on Alestes nurse in Tchad (a). Morphology of genitalia and hamuli haptors of sites. For instance, even though
the four species of Ligophorus parasitizing the Teleost Liza saliens in the Mediter- mankind has managed to elimi-
ranean (b). (Reproduced, with permission, from Ref. 16.) nate (almost) all of its competitors
and predators, current knowledge
indicates that it has been unable to
albicans16 suggests other modes of speciation instead eliminate any of its parasites (smallpox being the
of the classical allopatric model. exception that proves the rule). This is illustrated by
modern prophylactic campaigns against malaria that
Does the parasitic way of life favour phylogenic are followed by the emergence of more and more
diversification? Plasmodium strains resistant to nivaquine. As previ-
Parasitism represents the conquest of life by life. ously underlined45, this genetic variability is crucial
The living environment evolves continuously. Thus, in both therapy and susceptibility to immune attack.
in order to persist in their living environments para- There is a need to obtain the most precise knowledge
sites must continuously adapt to their hosts. Hosts of parasite diversity before developing therapeutics
represent a major part of the ecological needs of their or vaccines. In the same way, the identification of the
parasites (habitat, resource, etc.)40. Hosts may repre- existing diversity of parasitic organisms must be
sent many different kinds of resources and habitats taken into account in epidemiological surveys. This
(communities, species, populations, cohorts, sexes, may allow us to discriminate more effectively, within
individuals, organs, cells and molecules). Further- parasite communities, those that are pathogenic and
more, hosts develop defences against such intruders, those that are not. This can be illustrated by the gen-
by behavioural, physiological and demographic means. etic divergences found between strains of C. albicans,
Such defences impose an additional source of selec- which are comparable to that existing between the
tive and diversifying pressures on parasites. Such con- different mammalian species of the same genus16.
tinuous mutual aggressions resulting from the never- Moreover, genetic distances between C. albicans sam-
ending modifications of the living environment have pled in one human host46 exceeded that seen between
largely shaped the life history traits and the evolu- great apes and humans47, which diverged 5–7 million
tionary pathways in host–parasite systems (Red years ago48. In addition, when compared with the
Queen concept)41. protozoan species Trypanosoma cruzi, for example, the
The potential number of diversifying factors is overall genetic variability of the species C. albicans is at
much larger for parasitic organisms than for free- least four times lower (M. Tibayrenc, pers. commun.).
living organisms. All living species are involved in
parasitism, either as parasites or as hosts42 and, as Concluding remarks: many or no species concepts?
suggested by Timm and Clauson43, parasites consti- Providing a general and satisfactory species defini-
tute the main part of the known species diversity. tion appears to be a very difficult task, especially
That the parasitic way of life might be a diversifying given the very large number of potential applications
12 50 Parasitology Today, vol. 14, no. 1, 1998
 Reviews
with different functional requirements (taxonomy, or ‘clonal’ populations? Parasitol. Today 7, 232–235
conservation biology, functional ecology, evolution- 15 Pujol, C. et al. (1993) The yeast Candida albicans has a clonal
mode of reproduction in a population of infected human
ary biology and medicine). In fact, we do not believe immunodeficiency virus-positive patients. Proc. Natl. Acad. Sci.
that it is possible to reach a species definition that will U. S. A. 90, 9456–9459
satisfy everybody. In this paper, our aim is not to pro- 16 Euzet, L. and Combes, C. (1980) in Les Problèmes de l’Espèce dans
le Règne Animal (Vol. 3), Mem. Soc. Zool. 40, 238–285
vide a new species definition because we feel the 17 Werren, J.H. (1980) Sex ratio adaptations to local mate compe-
extant ones (typological, BSC, etc.) will continue to tition in a parasitic wasp. Science 208, 1157–1159
work in their different domains of application. Our 18 Combes, C. (1988) in L’Adaptation, Pour La Science, pp 166–173, Belin
goal is to draw attention to the fact that the most cur- 19 Brémond, P. et al. (1993) Argument en faveur d’une modi-
fication du génome (introgression) du parasite humain
rently used concept (the BSC) might not be very help- Schistosoma haematobium par les gènes de S. bovis, au Niger.
ful in parasitology, because of the reasons outlined C. R. Acad. Sci. Life Sci. 316, 667–670
above, and that it may prevent researchers from con- 20 Tchuem Tchuente, L.A. et al. (1993) Choice of mate, a repro-
sidering several evolutionary processes. The strong ductive isolating mechanism between Schistosoma intercalatum
and S. mansoni in mixed infections. Int. J. Parasitol. 23, 179–185
potential for diversification displayed by parasites, 21 Voltz, A. et al. (1988) Isoenzyme analysis of Echinostoma liei:
possibly due to the larger opportunities for sympatric Comparison and hybridization with other African species.
speciation in such groups, should allow parasitolo- Exp. Parasitol. 66, 13–17
gists to play a major role in different fields of biology. 22 Maynard-Smith, J. et al. (1991) Localised sex in bacteria. Nature
349, 29–31
In evolutionary biology, parasites appear as ideal 23 Heinemann, J.A. (1991) Genetics of gene transfer between
models for the study of specialization and speciation species. Trends Genet. 7, 181–185
and much can be learned from them. In phylogenetic 24 Agatsuma, T. et al. (1992) Electrophoretic evidence of a hybrid
studies the genetic consequences of such potential for origin for tetraploid Paragonimus westermani discovered in
north-eastern China. Parasitol. Res. 78, 537–538
diversification should allow different hypotheses, such 25 Fialkowski, K.R. (1988) Lottery of sympatric speciation. A com-
as the molecular clock, to be tested, in particular in puter model. J. Theor. Biol. 130, 379–390
groups where such a diversification is evident (eg. 26 De Meeûs, T. et al. (1993) Polymorphism in heterogeneous
monogeneans and bird lice). Too few such studies are environments, habitat selection and sympatric speciation: soft
and hard selection models. Evol. Ecol. 7, 175–198
available at the present time. Parasite communities 27 Johnson, P.A. et al. (1996) Conditions for sympatric speciation
should provide very useful models for studying the – a diploid model incorporating habitat fidelity and non-
interaction between species, competition and exclu- habitat assortative mating. Evol. Ecol. 10, 187–205
sion and biological diversity maintenance, because 28 Rice, W.R. and Salt, G.W. (1988) Speciation via disruptive
selection: experimental evidence. Evolution 131, 911–917
the ecological niche of a parasite will often be easier 29 Bush, G. L. (1992) Host race formation and sympatric speciation
to define (as it is concentrated in the host). In medi- in Rhagoletis fruit flies (Diptera: Tephrtidae). Psyche 99, 335–357
cine, the mechanisms involved in parasite diversific- 30 Marques, F. et al. (1995) Five new species of Acanthobothrium
ation (in the wide sense) should allow a better under- van Beneden, 1849 (Eucestoda: Tetraphyllidea: Onchobothri-
idae) in stingrays from the gulf of Nicoya, Costa Rica. J. Parasitol.
standing of eradication failures. Also, it should be 81, 942–951
considered more often that what appears to be a sin- 31 Dogiel, V.A. (1964) General Parasitology, Oliver and Boyd
gle pathogenic entity might actually comprise several 32 Ludwig, H.W. (1982) Host specificity in anoplura and coevolu-
very different genetic entities. As mentioned previ- tion of anoplura and mammalia. Mem. Mus. Natn. Hist. Nat.
Paris 123, 145–152
ously, the tremendous levels of genetic diversity found 33 Théron, A. and Combes, C. (1995) Asynchrony of infection tim-
within C. albicans and T. cruzi reveal that these taxa ing, habitat preference, and sympatric speciation of schisto-
are complex and surely made up of different biologi- some parasites. Evolution 49, 372–375
34 De Meeûs, T. et al. (1995) Maintenance of two genetic entities
cal entities (species). Because they co-exist, these dif- by habitat selection. Evol. Ecol. 9, 131–138
ferent biological entities might have different ecologi- 35 Wood, T.K. and Guttman, S.I. (1983) Euchenopa binotata com-
cal niches (ie. needs) and thus different sensitivities to plex: sympatric speciation? Science 220, 310–312
one or another treatment. 36 Craig, T.P. et al. (1993) Behavioural evidence for host-race for-
mation in Eurosta solidaginis. Evolution 47, 1696–1710
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3 Templeton, A.R. (1989) in Speciation and its Consequences (Otte, morphism, host races or sibling species? Heredity 75, 416–424
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there so many kinds of animal species? Am. Nat. 93, 145–159 40 Renaud, F. et al. (1996) Biodiversity and evolution in host–
5 Felsenstein, J. (1981) Skepticism towards Santa Rosalia, or why parasite associations. Biodiv. Conserv. 5, 963–974
are there so few kinds of animals? Evolution 35, 124–138 41 Van Valen, L. (1973) A new evolutionary law. Evol. Theor. 1, 1–30
6 Bush, G.L. (1993) in Evolutionary Patterns and Processes (Leeds, 42 Barbault, R. (1988) Population biology and evolutionary ecol-
D.R. and Edwards, D., eds), pp 229–249, Academic Press ogy in France: current state prospects. J. Evol. Biol. 1, 211–231
7 Lymbery, A.J. (1992) Interbreeding, monophyly and the Genetic 43 Timm, R.M. and Clauson, B.L. (1987) in Coevolution, pp 212–214,
Yardstick: species concepts in parasites. Parasitol. Today 8, 208–211 McGraw–Hill
8 Lymbery, A.J. and Thompson, R.C.A. (1996) Species of 44 Mitter, C. et al. (1988) The phylogenetic study of adaptive
Echinococcus: pattern and process. Parasitol. Today 12, 486–491 zones – has phytophagy promoted insect diversification? Am.
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ix–xviii, Transvaal Museum Monograph No. 4 45 Cox, F.E.G. (1991) Variation and vaccination. Nature 349, 193
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11 Futuyma, D.J. (1986) Evolutionary Biology (2nd edn), Sinauer multilocus enzyme electrophoresis analysis. FEMS Microbiol.
12 Bell, G. (1982) The Masterpiece of Nature, University of California Press Lett. 137, 269–273
13 Tibayrenc, M. and Ayala, F.J. (1991) Toward a population 47 Bruce, E.J. and Ayala, F.J. (1979) Phylogenetic relationships
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 Update TRENDS in Ecology and Evolution Vol.22 No.8 391

aspects of avian sex chromosome evolution that are 6 Shetty, S. et al. (1999) Comparative painting reveals strong
chromosome homology over 80 million years of bird evolution.
inevitable from those that are due strictly to chance.
Chrom. Res. 7, 289–295
Additionally, even though the palaeognathous sex 7 Charlesworth, B. (1991) The evolution of sex-chromosomes. Science
chromosomes are as old as those of the Neognathae, some- 251, 1030–1033
thing has slowed the process of sex chromosome evolution 8 Ellegren, H. and Carmichael, A. (2001) Multiple and independent
in the group. This presents a living series of slow-motion cessation of recombination between avian sex chromosomes.
Genetics 158, 325–331
time-shots in the progression of avian sex chromosomes,
9 Handley, L.L. et al. (2004) Evolutionary strata on the chicken Z
from the largely undifferentiated ostrich and emu Z and W, chromosome: implications for sex chromosome evolution. Genetics
to the distinguishably different intermediate tinamou Z 167, 367–376
and W, to the terminal neognathous sex chromosomes that 10 Tsuda, Y. et al. (2007) Comparison of the Z and W sex chromosomal
only recombine in a small and highly constrained pseudo- architectures in elegant chrested tinamou (Eudromia elegans) and
ostrich (Struthio camelus) and the process of sex chromosome
autosomal region (Figure 1). These characteristics offer a differentiation in palaeognathous birds. Chromosoma 116, 159–
powerful clade for the study of sex chromosome evolution, 173
which future sequence, linkage and cytogenetic analysis 11 Ogawa, A. et al. (1998) The location of Z- and W-linked marker genes
can exploit. and sequence on the homomorphic sex chromosomes of the ostrich and
the emu. Proc. Natl. Acad. Sci. U. S. A. 95, 4415–4418
Acknowledgements 12 Pigozzi, M.I. and Solari, A.J. (1999) The ZW pairs of two paleognath
We thank the Wenner-Gren Foundation and the Swedish Research birds from two orders show transitional stages of sex chromosome
Council for support, as well as two anonymous reviewers for helpful differentiation. Chrom. Res. 7, 541–551
suggestions. 13 Matsubara, K. et al. (2006) Evidence for different origin of sex
chromosomes in snakes, birds, and mammals and step-wise
differentiation of snake sex chromosomes. Proc. Natl. Acad. Sci. U.
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1 Bachtrog, D. (2006) A dynamic view of sex chromosome evolution. Curr.
14 de Kloet, R.S. and de Kloet, S.R. (2003) Evolution of the spindlin gene in
Opin. Genet. Dev. 16, 578–585
birds: independent cessation of the recombination of sex chromosomes
2 Ezaz, T. et al. (2006) Relationships between vertebrate ZW and XY sex
at the spindlin locus in neognathous birds and tinamous, a
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3 Ellegren, H. (2000) Evolution of the avian sex chromosomes and their
15 Berlin, S. and Ellegren, H. (2006) Fast accumulation of
role in sex determination. Trends Ecol. Evol. 15, 188–192
nonsynonymous mutations on the female-specific W chromosome in
4 Fridolfsson, A.K. et al. (1998) Evolution of the avian sex chromosomes
birds. J. Mol. Evol. 62, 66–72
from an ancestral pair of autosomes. Proc. Natl. Acad. Sci. U. S. A. 95,
8147–8152
5 van Tuinen, M. and Hedges, S.B. (2001) Calibration of avian molecular 0169-5347/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved.
clocks. Mol. Biol. Evol. 18, 206–213 doi:10.1016/j.tree.2007.05.003

Letters

Without morphology, cryptic species stay in

taxonomic crypsis following discovery
Birgit C. Schlick-Steiner1,2,3, Bernhard Seifert4, Christian Stauffer2, Erhard Christian1,
Ross H. Crozier3 and Florian M. Steiner1,2,3
1
Institute of Zoology, Department of Integrative Biology and Biodiversity Research, Boku, University of Natural Resources and
Applied Life Sciences Vienna, Gregor Mendel Str. 33, A-1180 Vienna, Austria
2
Institute of Forest Entomology, Forest Pathology and Forest Protection, Department of Forest and Soil Sciences, Boku, University
of Natural Resources and Applied Life Sciences Vienna, Hasenauerstr. 38, A-1190 Vienna, Austria
3
School of Marine and Tropical Biology, James Cook University, DB23, Townsville, Queensland 4811, Australia
4
State Museum of Natural History Görlitz, Post Box 300154, D-02806 Görlitz, Germany

Recently, Bickford et al. [1] highlighted the importance of taxonomically valid names on the basis of name-bearing
exploring cryptic diversity. Their biology-focused contri- specimens (types). Types often date back to Linnaeus’ time
bution is a reminder of the original questions regarding the and are frequently unsuitable for molecular studies,
current debate between molecular and traditional taxon- despite progress in this field [5], even setting aside that
omy [2], and a call for synergies between these approaches. museum curators usually refuse molecular sampling of
Only an integration of all disciplines can promote biological fragile type specimens. MOBAT can link cryptic species
research at the tempo set by the biodiversity crisis [3,4]. to Linnean nomenclature and to established biological
But one point is left unemphasized: the undiminished knowledge. Once discovered, many cryptic species can be
relevance of morphology-based alpha taxonomy (MOBAT), identified by means of external physical characters [6],
which is still the most important discipline for assigning especially with methods of morphometric statistics [7].
Badly under-resourced [8], MOBAT cannot keep pace
Corresponding author: Schlick-Steiner, B.C. (birgit.florian@gmail.com).
Available online 15 June 2007. with the discovery of cryptic species, as illustrated by a
54
www.sciencedirect.com
392 Update TRENDS in Ecology and Evolution Vol.22 No.8

topical example. An integrative approach revealed at least tions for evolutionary theory, biogeography and conserva-
seven sympatric species hidden in two nominal species of tion planning’ [1] is to be realised.
western Palearctic Tetramorium ants [9]. Because most of
these species are both common and widespread, it is risky to References
guess which were used for types by previous taxonomists; 1 Bickford, D. et al. (2007) Cryptic species as a window on diversity and
conservation. Trends Ecol. Evol. 22, 148–155
approximately 50 taxon names in synonymy, and their types 2 Smith, V.S. (2005) DNA barcoding: perspectives from a ‘Partnerships for
(the oldest from 1850), demand scrutiny [10]. More than 500 Enhancing Expertise in Taxonomy’ (PEET) debate. Syst. Biol. 54, 841–
publications over 150 years contain information on life 844
history, ethology, social biology, semiochemistry, ecology 3 Will, K.W. et al. (2005) The perils of DNA barcoding and the need for
and invasion biology of these ant species. But of which integrative taxonomy. Syst. Biol. 54, 844–851
4 Whitfield, J. (2007) We are family. Nature 446, 247–249
ant species? Biological knowledge that would help elucidate 5 Hajibabaei, M. et al. (2006) A minimalist barcode can identify a
patterns and consequences of cryptic diversification [1] lies specimen whose DNA is degraded. Mol. Ecol. Notes 6, 959–964
idle. Only analysing historical voucher material could tap 6 Saez, A.G. and Lozano, E. (2005) Body doubles. Nature 433, 111
these resources. However, the current working capacity of 7 Seifert, B. (2002) How to distinguish most similar insect species –
improving the stereomicroscopic and mathematical evaluation of
ant MOBAT is slight. Just two of >200 European myrme-
external characters by example of ants. J. Appl. Entomol. 126, 1–9
cologists work in numerical MOBAT as full-time pro- 8 Wheeler, Q.D. et al. (2004) Taxonomy: impediment or expedient? Science
fessionals. We guess that the situation is similar with 303, 285
other groups of organisms. While the discovery of cryptic 9 Schlick-Steiner, B.C. et al. (2006) A multidisciplinary approach
species increases exponentially [1], the number of experi- reveals cryptic diversity in western Palaearctic Tetramorium ants
(Hymenoptera: Formicidae). Mol. Phylogenet. Evol. 40, 259–273
enced MOBATists stagnates.
10 Bolton, B. et al. (2007) Bolton’s catalogue of ants of the world: 1758–
Even when uncovered by modern methods, many cryptic 2005. Harvard University Press
species remain taxonomically cryptic. Investment in all
disciplines contributing to integrative taxonomy, including 0169-5347/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved.
MOBAT, is essential if the promise of ‘profound implica- doi:10.1016/j.tree.2007.05.004

Book Review

Laws on growth and heat

In the Beat of a Heart: Life, Energy and the Unity of Nature by John Whitfield. Joseph Henry Press, 2006. US$ 27.95 hbk (270 pages)
ISBN 0309096812

Jaap van der Meer

Department of Marine Ecology and Evolution, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB Den Burg
(Texel), the Netherlands

Organisms as diverse as yeast and moose Beginning with an historical account, d’Arcy Thompson
show striking similarities in their growth is introduced as the godfather of mathematical thinking in
trajectories, initially growing quickly, but biology. In a letter to a former student Thompson writes
then gradually slowing their growth as that, to understand growth patterns in foraminifera, ‘I
they get larger, eventually stopping altog- have taken to Mathematics . . .’. This quote is the leitmotiv
ether. They also follow Kleiber’s rule; that of Whitfield’s book, culminating in a modern version in
is, their metabolic rate is proportional to which Brown and Enquist did not literary ‘take Mathemat-
their mass raised to the 3/ 4 power. Many ics’, but joined forces with West. However, before these
scholars have tried to find laws valid for contemporaries are discussed, their predecessors in the
all life forms that could explain these two quest are presented. Max Rubner, Max Kleiber and Lud-
regularities, but none have yet convinced the scientific wig von Bertalanffy feature, among many others.
community as a whole. By the end of the previous century, Such mix of an historical sketch and a description of the
the subject was receiving little if any attention; however, lives and work of present-day scientists who have only
work by the physicist Geoffrey West and ecologists Jim recently launched ideas that are still debated, is, for
Brown and Brian Enquist has since revitalized the topic various reasons, a risky exercise. I found it amusing to
[1,2]. John Whitfield, an evolutionary biologist turned read that 18 years after signing a contract on a second
science writer, has followed their work and, following a edition of On Growth and Form, Thompson received a
popular paper [3], his debut science book In the Beat of a letter from his publisher with the remark ‘I must warn
Heart explores the quest for general laws on metabolism you that you have already slightly exceeded the correction
and growth. allowance . . .’. I find it less diverting to hear that my
contemporaries always buy lots of beer when they go on
Corresponding author: van der Meer, J. (jaap.vander.meer@hetnet.nl). a field trip or that they are ‘foaming at the mouth of
Available online 9 May 2007. excitement’ when they discuss their own ideas. But this
55
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Lecturas traducidas. Laboratorio de Evolución, Facultad de Ciencias ______________________________________ 1

El significado de especie y de especiación:

una perspectiva genética.
Alan R. Templeton.
INTRODUCCIÓN

¿Qué es una especie? Esta cuestión fundamental debe ser respondida antes de que el
proceso de formación de las especies pueda ser investigado. Como cualquier vistazo general
a la literatura evolutiva rápidamente revelará, existen muchas definiciones de especie. Estas
diferentes definiciones reflejan los diversos tipos de preguntas evolutivas y/o de organismos
con los cuales sus autores estaban principalmente interesados. En consecuencia, un concepto
de especie sólo puede ser evaluado en términos de una meta o propósito particular. Mi meta
es entender la especiación como un proceso genético evolutivo. Una asunción fundamental
tras esta meta es que para la especiación, independientemente de una definición precisa de
especie, lo mejor es una aproximación mecanística examinando las fuerzas evolutivas que
operan sobre los individuos dentro de poblaciones o subpoblaciones y siguiendo sus efectos
hacia arriba hasta que en último término causen que todos los miembros de esa población o
subpoblación adquieran atributos fenotípicos que le confieran al grupo el status de especie.
Este énfasis en los mecanismos evolutivos genéticos que operan dentro de las
poblaciones de individuos ubica completamente a la especiación dentro del dominio de la
genética de poblaciones. De acuerdo con esto, lo que se requiere es un concepto de especie
que pueda ser relacionado directamente con el marco mecanístico de la genética de
poblaciones. Para alcanzar esta meta, repasaré en primer lugar tres conceptos de especie que
poseen fuertes partidarios en la literatura actual: el concepto evolutivo de especie, el
concepto biológico de especie, y el concepto de especie de reconocimiento. Todos estos
conceptos de especie consideran a las especies como entidades biológicas reales e intentan
definir a las especies en términos de alguna propiedad biológica fundamental. En este
aspecto, todas estas definiciones son conceptos biológicos de especie, aunque una de ellas es
referida usualmente como ‘el concepto biológico de especie’. Dado que ‘el concepto
biológico de especie’ define a las especies en términos de mecanismos de aislamiento, es
mejor conocida como el concepto de aislamiento (Patterson, 1985). La terminología de
Patterson será utilizada en el resto de este capítulo.
Luego de revisar los puntos fuertes y los débiles de estos tres conceptos, propondré
un cuarto concepto biológico de especie, el concepto de cohesión, el cual intenta utilizar los
puntos fuertes de los otros tres mientras evita sus puntos débiles con respecto a la meta de
definir las especies de una forma que sea compatible con el marco mecanístico de la
genética de poblaciones. De esta manera, puede lograrse una definición de especie que
ilumine, en vez de oscurecer o desencaminar, a los mecanismos de especiación y a sus
consecuencias genéticas.

TRES CONCEPTOS BIOLÓGICOS DE ESPECIE

El concepto evolutivo de especie.

Bajo esta definición, una especie consiste en una población o grupo de poblaciones
que comparten un destino evolutivo común a través del tiempo. Esta definición tiene la
ventaja de ser aplicable tanto a grupos vivientes como a grupos extintos y a organismos
sexuados y asexuados. Además, pone énfasis en el hecho de que una unidad de especie
puede mantenerse unida no sólo a través del flujo génico sino también a través de
restricciones del desarrollo, genéticas y ecológicas. Finalmente, este concepto es útil debido

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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a que se asemeja a la definición operacional de especie utilizada por la mayoría de los

taxónomos y paleontólogos en ejercicio. Las decisiones de dar status de especie se toman
usualmente en base a patrones de cohesión fenotípica dentro de un grupo de organismos
versus la discontinuidad fenotípica entre los grupos. Sin embargo, cuando se estudia una
variedad de fenotipos, a menudo se descubre que los patrones de cohesión/discontinuidad
varían en función del fenotipo que se mida. Una falla del concepto evolutivo de especie es
que provee poca o ninguna guía acerca de cuáles son los rasgos más importantes en la
definición de las especies.
Existen otras dos dificultades principales con este concepto. En primer lugar, está el
problema de juzgar qué constituye un destino evolutivo ‘común’. Obviamente, los
polimorfismos pueden existir incluso dentro de las poblaciones locales, y muchas especies
son politípicas. Debido a esto, destino evolutivo ‘común’ no significa ‘idéntico’, por lo cual
debe hacerse algún juicio acerca de cuánta diversidad se permite dentro de un destino
evolutivo ‘común’. Finalmente, y lo más importante en relación a la meta de este capítulo, el
concepto evolutivo de especie no es una definición mecanística. Trata sólo con la
manifestación de la cohesión en vez de con los mecanismos evolutivos responsables de tal
cohesión. Por lo tanto, no provee un marco adecuado para la integración de factores de la
genética de poblaciones dentro del concepto de especie.

El concepto de especie de aislamiento.

El concepto de especie dominante en gran parte de la literatura evolutiva es conocido

popularmente como el concepto biológico de especie. Mayr (1963) definió el concepto de
especie de aislamiento como ‘grupos de poblaciones naturales actual o potencialmente
capaces de entrecruzamiento que se encuentran aisladas reproductivamente de otros grupos
similares.’ De forma similar, Dobzhansky (1970) afirmó que ‘Las especies son sistemas de
poblaciones: el intercambio genético entre estos sistemas se encuentra limitado o impedido
por un mecanismo de aislamiento reproductivo o quizás por una combinación de varios de
estos mecanismos.’ Como White (1978) ha subrayado, el concepto de aislamiento de especie
‘es al mismo tiempo una comunidad reproductiva, un pool de genes, y un sistema genético.’
Son estos dos últimos atributos los que hacen a este concepto de especie particularmente útil
para la integración de consideraciones de la genética de poblaciones en el problema del
origen de las especies. La genética de poblaciones se ocupa de las fuerzas evolutivas que
operan en los pools de genes y de los tipos de sistemas genéticos que surgen luego de que
operen estas fuerzas. El concepto de aislamiento de especie es por tanto potencialmente útil
en el análisis de la especiación desde la perspectiva de la genética poblacional, pero
desafortunadamente posee algunas serias dificultades que deben ser rectificadas antes de que
este potencial pueda ser comprendido.
Estas dificultades surgen del hecho de que este concepto de especie se define en
términos de mecanismos de aislamiento. La Tabla 1 presenta una breve clasificación de los
tipos de barreras de aislamiento, y tablas similares pueden encontrarse en cualquier libro
sobre especiación de Mayr o Dobzhansky. Bajo el concepto de especie de aislamiento, estas
barreras de aislamiento definen las fronteras de la comunidad reproductiva y del pool de
genes y preservan la integridad del sistema genético de la especie.
TABLA 1. Clasificación de los mecanismos de aislamiento.
1. Mecanismos precopulatorios que impiden los cruzamientos interpoblacionales
a. Aislamiento ecológico o de hábitat: las poblaciones se aparean en distintos hábitats en
la misma región
general, o utilizan distintos agentes polinizadores, etc.
b. Aislamiento temporal: las poblaciones se aparean en distintos momentos del año.

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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c. Aislamiento etológico: parejas potenciales de distintas poblaciones se encuentran pero

no se aparean.
2. Aislamiento postcopulatorio pero precigótico
a. Aislamiento mecánico: ocurren apareamientos interpoblacionales pero no tiene lugar
la transferencia de
esperma.
b. Mortalidad gamética o incompatibilidad: ocurre transferencia de esperma pero el
óvulo no es
fertilizado.
3. Aislamiento postcigótico
a. Inviabilidad de la F1: los cigotos híbridos poseen viabilidad reducida.
b. Esterilidad de la F1: los adultos híbridos poseen fertilidad reducida.
c. Decaimiento de los híbridos: los híbridos de la F2 o de los retrocruzamientos poseen
viabilidad
o fertilidad reducida.
d. Interacciones coevolutivas o citoplasmáticas: los individuos de una población infectada
por un endoparásito o con un elemento citoplasmático particular son fértiles entre ellos pero
la viabilidad y/o la fertilidad decaen cuando los apareamientos ocurren entre individuos
infectados y no infectados.

Paterson (1985) ha señalado que una dificultad fundamental con el concepto de

especie de aislamiento es que conduce a error cuando se piensa en el proceso de especiación.
Por ejemplo, bajo el clásico modelo alopátrido de especiación, la especiación ocurre cuando
las poblaciones se encuentran totalmente separadas una de la otra por barreras geográficas.
Los mecanismos de aislamiento intrínsecos dados en la Tabla 1 son obviamente irrelevantes
como barreras de aislamiento durante la especiación debido a que en alopatría no pueden
funcionar como mecanismos de aislamiento. Por tanto, las fuerzas evolutivas responsables
de este proceso de especiación alopátrida no tienen nada que ver con el ‘aislamiento’. Esto
también se aplica a otros mecanismos de especiación (Templeton, 1981). Esto no significa
que el aislamiento no sea un producto del proceso de especiación en algunos casos, pero el
producto (i.e., el aislamiento) no debe ser confundido con el proceso (i.e., la especiación). El
concepto de aislamiento a sido perjudicial en los estudios de especiación precisamente
porque ha fomentado esta confusión (Paterson, 1985).

El concepto de especie de reconocimiento.

Paterson (1985) ha argumentado fuertemente que esta confusión puede ser evitada
viendo a los así llamados mecanismos de aislamiento desde otra perspectiva. Por ejemplo,
considérense los mecanismos de aislamiento precopulatorios listados en la Tabla 1. En la
literatura evolutiva es común hallar afirmaciones de que complejos rituales de cortejo,
señales para el apareamiento, etc. funcionan como barreras de aislamiento precopulatorias
que existen para impedir la hibridación con otras especies. Los trabajos de Dobzhansky
(1970) indican cuán dominante era esta idea en el pensamiento de uno de los principales
arquitectos y proponentes del concepto biológico de especie. No obstante, como Tinbergen
(1953) señaló, tales mecanismos precopulatorios tienen varias funciones además del
aislamiento: la supresión o escape del comportamiento agresivo en el animal cortejado, la
sincronización de las actividades del apareamiento, la persuasión de la pareja potencial para
continuar con el cortejo, la coordinación en el tiempo y en el espacio del patrón de

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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apareamiento, la orientación de parejas potenciales para la cópula, y, finalmente, la propia

fecundación. La importancia de estas otras funciones del comportamiento precopulatorio es
ilustrada por el trabajo de Crews (1983) acerca del cortejo pseudomasculino y el
comportamiento copulatorio del lagarto partenogenético sin machos, Cnemidophorus
uniparens. En estos lagartos, la inseminación y el aislamiento precopulatorio son totalmente
irrelevantes ya que la reproducción es estrictamente partenogenética. Aún así, las hembras
muestran elaborados comportamientos de cortejo que se asemejan al cortejo de los machos
de especies cercanamente emparentadas. Estos comportamientos sirven como iniciador
neuroendócrino que coordina los eventos reproductivos. Obviamente, las conductas de
apareamiento facilitan la reproducción en estos lagartos, pero el aislamiento es irrelevante.
La pregunta crítica se convierte entonces en ¿cuál de éstas varias funciones (o cuál
combinación) es importante en el proceso de especiación? Paterson (1985) ha argumentado
que el aislamiento es una función irrelevante en el proceso de especiación. En consecuencia,
para examinar la razón de porqué surge una barrera ‘de aislamiento’ precopulatoria, es
necesario focalizar la atención en las otras funciones de estos mecanismos precopulatorios y
examinar las fuerzas evolutivas que operan sobre estas funciones (Paterson, 1985). Desde
este punto de vista, todas las otras funciones de estos comportamientos precopulatorios
pueden entenderse como facilitando la reproducción, no obstaculizándola como sucedía con
la función del aislamiento. La función del aislamiento puede surgir de hecho como un efecto
secundario de la evolución de las otras funciones, pero en general no es una parte activa del
proceso de especiación.
En consecuencia, los mecanismos de aislamiento constituyen una forma de pensar
acerca del proceso de especiación que conduce a error. Aunque todos los mecanismos
listados en la Tabla 1 se definen en términos de impedir la reproducción entre las
poblaciones, pueden también ser pensados de un modo intraespecífico como facilitando la
reproducción dentro de las poblaciones. En general, es esta inversión positiva de las
funciones dadas en la Tabla 1 la que juega el rol principal en la especiación. Paterson (1985)
se centró en la función positiva de estos mecanismos en la facilitación de la reproducción
entre los miembros de una cierta población. De acuerdo con esto, Paterson acepta la
premisa, compartida con el concepto de aislamiento, de que una especie es un campo para la
recombinación génica. A diferencia del concepto de aislamiento, el cual define los límites de
este campo en un sentido negativo a través de mecanismos de aislamiento, Paterson define
los límites de este campo en un sentido positivo a través de mecanismos de fertilización, es
decir, adaptaciones que contribuyen en los procesos de meiosis y fecundación. Las especies
se definen como la población más inclusiva de organismos biparentales individuales que
comparten un sistema de fertilización común.
En cierto sentido, los conceptos de especie de aislamiento y de reconocimiento son
las dos caras de una misma moneda. Dar vuelta la moneda es provechoso porque el concepto
de reconocimiento da una visión más clara de los procesos versus el patrón evolutivos,
mientras que el concepto de aislamiento conduce activamente a un error. Por tanto, dada la
meta de definir la especie de tal manera que facilite el estudio de la especiación como
proceso evolutivo, el concepto de reconocimiento es claramente superior al de aislamiento.
Paterson (1985) ha cargado al concepto de reconocimiento con varias restricciones
que no provienen necesariamente de su definición primaria. La más seria de éstas es el uso
exclusivo de los mecanismos de fertilización para definir una especie. Obviamente, un
campo de recombinación génica requiere más que la fertilización; requiere un ciclo de vida
completo en el cual los productos de la fertilización sean viables y fértiles. Además, los así
llamados mecanismos ‘de fertilización’ de Paterson poseen otras funciones evolutivas que él
ignora, como está bien ilustrado por el comportamiento de cortejo previamente discutido de
los lagartos partenogenéticos. Por tanto, así como Paterson criticó a los mecanismos de

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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Lecturas traducidas. Laboratorio de Evolución, Facultad de Ciencias ______________________________________ 5

aislamiento porque éstos podían evolucionar por razones distintas al aislamiento, sus
mecanismos ‘de fertilización’ de igual forma pueden evolucionar por razones distintas a la
fertilización.
Puede hacerse otra crítica menor al concepto de Paterson (Templeton, 1987), pero
deseo concentrarme en dos dificultades serias y fundamentales que comparten ambos
conceptos, el de aislamiento y el de reconocimiento. Como muchos otros problemas en el
mundo biológico, estos problemas son causados por el sexo -o demasiado, o demasiado
poco.

RESTRICCIONES SEXUALES DE LOS CONCEPTOS DE AISLAMIENTO Y DE

RECONOCIMIENTO.

Demasiado poco sexo.

Tanto el concepto de especie de aislamiento como el de reconocimiento sólo se

aplican a organismos que se reproducen sexualmente (Vrba, 1985). De acuerdo con esto,
grandes porciones del mundo orgánico quedan fuera del dominio lógico de estas
definiciones de especie. Esta es una seria dificultad para las personas que trabajan con
organismos partenogenéticos o asexuales.
Un aspecto particularmente problemático de la exclusión de las especies asexuadas
es que la mayoría de las ‘especies’ partenogenéticas despliegan los mismos patrones de
cohesión fenotípica dentro de ellas y de discontinuidad entre ellas que las especies sexuadas.
Por ejemplo, Holman (1987) examinó cómo podían reconocerse las especies sexuadas y las
especies asexuadas de rotíferos. Contrariamente a las predicciones hechas por el concepto de
aislamiento, descubrió que las especies en los taxa asexuados eran de hecho
consistentemente más reconocibles que aquellas de los taxa sexuados. Por consiguiente,
concluyó que para los rotíferos asexuales ‘las especies son reales y pueden ser mantenidas
por factores no reproductivos.’ Como ilustra este ejemplo, el mundo asexual se encuentra en
su mayor parte tan bien subdividido (o quizás mejor) en taxa biológicos fácilmente definidos
como lo está el mundo sexual. Esta realidad biológica no debería ser ignorada.
Ignorar a los taxa asexuales es una falla importante de los conceptos de aislamiento y
de reconocimiento, pero esta falla es en realidad más extensa que lo que mucha gente cree.
Por ejemplo, la genética evolutiva de las poblaciones con autofecundación es simplemente
un caso especial de poblaciones partenogenéticas automícticas (ej., ver Templeton, 1974a).
Por tanto, las especies con autofecundación también se encuentran fuera del dominio lógico
de los conceptos de aislamiento y de reconocimiento. Pero el problema no termina con las
especies con autofecundación. Por ejemplo, muchas especies de avispas poseen
apareamientos obligados entre hermanos (Karlin y Lessard, 1986). Tal sistema de
apareamiento, así como cualquier otro sistema cerrado de apareamiento, desplegará una
dinámica evolutiva que puede ser considerada como un caso especial de automixis, tal como
la autofecundación. Por tanto, todos los taxa sexuados con un sistema cerrado de
apareamiento se encuentran por fuera del dominio lógico de los conceptos de aislamiento y
de reconocimiento.
El problema no termina aquí, sin embargo. Los modelos para el análisis de la
selección multilocus en poblaciones automícticas y con autofecundación fueron aplicados
con mucho éxito a una población de cebada que poseía un 99.43% de autofecundación
(Templeton, 1974b). La razón de este éxito es bien clara: con tanta autofecundación , la
dinámica evolutiva de la población se aproximó mucho a la de una población 100%
autofecundante. Cuando la exogamia se encuentra en un nivel tan bajo, su rol principal es el

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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de introducir variabilidad genética dentro de la población. Una vez introducida, el destino

evolutivo de esa variación se asemeja más al de una población autofecundante que al de una
población exogámica. Además, el impacto genético de la exogamia ocasional es reducido
aún más por el aislamiento por distancia, lo que provoca que la mayor parte de la exogamia
ocurra entre individuos casi genéticamente idénticos. En consecuencia, desde la perspectiva
de la genética de poblaciones, esta población de cebada no puede ser considerada de ninguna
manera como un ‘campo para la recombinación génica’, y entonces yace fuera del dominio
lógico tanto del concepto de aislamiento como del de reconocimiento.
El problema del aislamiento por distancia previamente mencionado crea una
restricción más en el dominio lógico de los conceptos de aislamiento y de reconocimiento.
Una población exogámica caracterizada por un flujo génico muy limitado y tamaños
efectivos poblacionales pequeños tendrá casi las mismas consecuencias genéticas y la misma
dinámica evolutiva que una población predominantemente autofecundante. Ehrlich y Raven
(1969) estuvieron entre los primeros en señalar en términos fuertes que muchas especies
animales y vegetales no pueden ser consideradas como campo para la recombinación génica
en ningún sentido significativo con respecto a los mecanismos evolutivos básicos, y por lo
tanto también se encuentran por fuera del dominio lógico de los conceptos de aislamiento y
de reconocimiento.
El ejemplo de la cebada conduce a una pregunta interesante. Si una población con un
99,47% de autofecundación se encuentra fuera del dominio lógico de los conceptos de
aislamiento y de reconocimiento, ¿qué ocurre con una población con un 99% o con un 95%
de autofecundación? El trabajo de Ehrlich y Raven (1969) conduce a un conjunto de
preguntas similares: ¿en qué punto son el aislamiento por distancia y la subdivisión
poblacional suficientemente débiles como para incluir a un taxa dentro del dominio lógico
de los conceptos de aislamiento y de reconocimiento? A pesar de que no se trata de una
pregunta fácil de responder, el problema de los taxa genéticamente cerrados es a menudo
descartado en una o dos frases, siendo los taxa sexual o genéticamente cerrados tratados
como tipos de categorías distintivas (por ej., Mayr 1970; Vrba 1985). Sin embargo, desde el
punto de vista de los mecanismos evolutivos (y, por tanto, desde el punto de vista de la
especiación como proceso evolutivo), existe un continuo desde la dinámica evolutiva
panmíctica hasta la dinámica evolutiva genéticamente cerrada. En consecuencia, el dominio
lógico de los conceptos de aislamiento y de reconocimiento no está en absoluto claro ni bien
definido. La única certeza es que este dominio es mucho más restrictivo y limitado que lo
que en general se percibe.

Demasiado sexo.

Como se ha discutido, los sistemas reproductivos genéticamente cerrados causan

serias dificultades a los conceptos de aislamiento y de reconocimiento, pero también lo
hacen los sistemas genéticamente abiertos. Por ejemplo, Grant (1957), uno de los más
fuertes partidarios entre los botánicos del concepto de aislamiento, concluyó que menos del
50% de las especies exogámicas de 11 géneros de plantas californianas estaban bien
delimitadas por el aislamiento de otras especies. Una y otra vez en las plantas, los
taxónomos han definido especies que existen en grandes unidades conocidas como especies
singámicas (“syngameons”) que se caracterizan por una hibridación natural y un intercambio
genético limitado. Grant (1981) define a las especies singámicas como ‘la unidad más
inclusiva de entrecruzamiento en un grupo de especies con hibridación.’ La existencia
frecuente de especies singámicas en las plantas crea serias dificultades tanto para el
concepto de aislamiento como para el de reconocimiento debido a que el campo de la

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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recombinación genética es obviamente mayor que la especie taxonómica y que los grupos
que se comportan como entidades evolutivamente independientes. Una solución es
simplemente negar el status de especie de los miembros del grupo de especies singámicas.
Por ejemplo, Grant (1981) se refiere a los miembros del grupo de las especies singámicas
como ‘semiespecies’. Bajo el concepto de reconocimiento, el propio grupo de especies
singámicas sería la especie, dado que la definición de especie singámica de Grant es
virtualmente idéntica a la definición de especie de Paterson (1985). Sin embargo, los
botánicos no han tomado estas decisiones taxonómicas arbitrariamente. Las especies dentro
de un grupo singámico son a menudo unidades reales en términos de morfología, ecología,
genética y evolución. Por ejemplo, el registro fósil indica que dos especies de álamos
americanos (los ‘balsam poplars’ y los ‘cottonwoods’, ambos del género Populus) han
divergido hace al menos 12 millones de años y han generado híbridos a lo largo de este
período (Eckenwalder, 1984). Aún cuando los híbridos se encuentran muy extendidos, son
fértiles y antiguos, estas especies de árboles poseen y mantienen una cohesión genética,
fenotípica y ecológica entre ellas y una distinción que las separa y se han mantenido como
linajes evolutivos distintivos por al menos 12 millones de años (Eckenwalder, 1984). Por
tanto, estos álamos son unidades biológicas reales que no deberían ser ignoradas.
Es común en los zoólogos reconocer que el concepto de aislamiento posee
dificultades cuando es aplicado a las plantas superiores, exogámicas, pero luego argumentar
que el concepto de aislamiento funciona razonablemente bien para animales multicelulares
que se reproducen sexualmente. Sin embargo, esta visión ya no puede ser sostenida con la
creciente resolución que proveen las técnicas del ADN recombinante. Por ejemplo, en
mamíferos, se están llevando a cabo estudios en mi laboratorio en babuinos, ganado salvaje,
cánidos, roedores subterráneos y ratas, ejemplos, respectivamente, de primates, ungulados,
carnívoros y roedores -los cuatro grupos principales de mamíferos. En cada caso, existe
evidencia de que ocurre hibridación interespecífica en forma natural (Baker et al., 1989;
Davis et al., 1988; datos no publicados). A pesar de la hibridación, muchas de las unidades
taxonómicas dentro de estos grupos representan unidades biológicas reales en el sentido
morfológico, ecológico, genético y evolutivo. Por ejemplo, los lobos y los coyotes pueden
formar híbridos, y de hecho lo hacen. No obstante, son bastante distinguibles
morfológicamente unos de otros, poseen comportamientos extremadamente diferentes en
términos de estructura social y caza, y representan linajes evolutivos distintivos con
diferencias genéticas diagnósticas (Figura 1). Además, el registro fósil indica que han
evolucionado como linajes distintivos y continuos por al menos 0,5 millones de años (Hall,
1978) y quizás por tanto tiempo como 2 millones de años (Nowak, 1978). Aunque estos taxa
no satisfacen el criterio del concepto de especie por aislamiento, Hall (1978) argumenta que
son grupos biológicamente reales y que el status de especie es claramente apropiado.
Las especies singámicas animales no se encuentran de ninguna manera limitadas a
los mamíferos. Drosophila heteroneura y D. silvestris son dos especies hawaianas de
Drosophila con las cuales hemos trabajado. Aunque son filogenéticamente muy cercanas y
en gran medida simpátridas en la isla de Hawaii (Carson, 1978), son extremadamente
distinguibles morfológicamente, siendo la diferencia más dramática que silvestris posee una
cabeza redonda y heteroneura una cabeza con forma de martillo (Val, 1977). Pueden ser
hibridadas en el laboratorio, y los híbridos y los F2 y retrocruzamientos subsiguientes son
completamente fértiles y viables (Val, 1977; Templeton, 1977; Ahearn y Templeton, 1989).
Debido a que la morfología de los híbridos es conocida gracias a estos estudios de
laboratorio, Kaneshiro y Val (1977) fueron capaces de descubrir que la hibridación
interespecífica ocurre en la naturaleza. Nuestros estudios moleculares (DeSalle y Templeton,
1987) confirmaron que los híbridos realmente se forman en la naturaleza, y, lo que es más,
que estos híbridos pueden retrocruzarse, y de hecho lo hacen, hasta tal punto que un

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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haplotipo mitocondrial de heteroneura puede hallarse asociado a una morfología

aparentemente normal de silvestris. A pesar de esta hibridación natural, las especies pueden
mantener, y lo hacen, sus muy distinguibles morfologías de base genética (Templeton, 1977;
Val, 1977) y poseer distintas filogenias de su ADN nuclear (Hunt y Carson, 1983; Hunt et
al., 1984) a pesar de la limitada introgresión observada con el ADN mitocondrial (DeSalle et
al., 1986). Por tanto, tanto la morfología como las moléculas definen a estos taxa como
linajes reales y evolutivamente distinguibles.
Como ilustran estos y otros estudios, los taxa animales despliegan frecuentemente la
hibridación natural que produce híbridos fértiles y viables. Estos taxa se han reconocido
usualmente como especies debido a sus morfologías y ecologías distintivas y debido a que
los estudios moleculares modernos han revelado que se comportan como linajes evolutivos
independientes, al menos con respecto a sus genomas nucleares. En otras palabras, muchas
especies animales son miembros de grupos singámicos, tal como lo son las plantas. Por
tanto, las especies singámicas son un problema extendido para los conceptos de aislamiento
y de reconocimiento.

EL CONCEPTO COHESIVO DE ESPECIE.

Ahora es posible una nueva definición biológica de especie, la que llamo el concepto
cohesivo de especie. La especie en el concepto cohesivo es la población más inclusiva de
individuos que poseen el potencial para la cohesión fenotípica a través de mecanismos
intrínsecos de cohesión (Tabla 2). Trataré ahora sobre el significado de este concepto de
especie, mostrando cómo toma partes prestadas de los conceptos evolutivo, de aislamiento y
de reconocimiento, mientras que evita sus serios defectos.
Al igual que el concepto evolutivo de especie, el concepto cohesivo de especie define
a la especie en términos de cohesión genética y fenotípica. Como consecuencia, el concepto
de cohesión comparte con el concepto evolutivo su fortaleza de poder ser aplicable a los taxa
que se reproducen asexualmente (o por intermedio de otros sistemas cerrados o casi cerrados
de apareamiento), y a los taxa que pertenecen a grupos singámicos. Al contrario que el
concepto evolutivo de especie, el concepto de cohesión define a las especies en términos de
los mecanismos que producen la cohesión más que de la manifestación de la cohesión en el
tiempo evolutivo. Este es un enfoque mecanístico similar al que toma el concepto de
aislamiento, si bien en este caso el foco se encuentra sobre mecanismos de cohesión en vez
de mecanismos de aislamiento. Al definir una especie en términos de mecanismos de
cohesión, el concepto cohesivo puede ser fácilmente relacionado con un marco mecanístico
de genética de poblaciones y puede guiar en la comprensión de la especiación como proceso
evolutivo. En particular, la especiación es ahora considerada como la evolución de los
mecanismos de cohesión (como opuestos a los mecanismos de aislamiento). Esto significa
también que el concepto de cohesión se centra principalmente en los taxa vivientes más que
en los taxa fósiles.

TABLA 2. Clasificación de los mecanismos de cohesión.

I. Intercambiabilidad genética: los factores que definen los límites de dispersión de las
nuevas variantes
génicas a través del flujo génico.
A. Mecanismos que promueven la identidad genética a través del flujo génico
1. Sistema de fertilización: los organismos son capaces de intercambiar gametos que
conduzcan a una
fecundación exitosa.

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
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2. Sistema de desarrollo: los productos de la fertilización son capaces de producir

adultos viables y
fértiles.
B. Mecanismos de aislamiento: la identidad genética se pereserva por la falta de flujo
génico con otros
grupos.
II. Intercambiabilidad demográfica: los factores que definen el nicho fundamental y los
límites de dispesión
de las nuevas variantes génicas a través de la deriva genética y la selección natural.
A. Reemplazabilidad: la deriva genética (la descendencia de un ancestro común)
promueve la identidad
genética.
B. Desplazabilidad:
1. Fijación selectiva: la selección natural promueve la identidad genética favoreciendo
la fijación de
una variante genética.
2. Transiciones adaptativas: la selección natural favorece a las adaptaciones que
alteran directamente a
la intercambiabilidad demográfica. La transición está restringida por:
a. Restricciones mutacionales en el origen de la variación fenotípica heredable.
b. Restricciones en el destino de la variación heredable
i. Restricciones ecológicas.
ii. Restricciones del desarrollo.
iii. Restricciones históricas.
iv. Restricciones de la genética poblacional.

Como fue señalado por Paterson (1985), es útil definir los mecanismos subyacentes
al status de especie de tal forma que las definiciones reflejen la función evolutiva más
probable de los mecanismos durante el proceso de especiación. De acuerdo con esto, los
mecanismos de cohesión serán definidos para que reflejen su función evolutiva más
probable. La tarea básica es identificar esos mecanismos de cohesión que contribuyen a
mantener a un grupo como un linaje evolutivo. La esencia misma de un linaje evolutivo
desde una perspectiva de la genética poblacional es que nuevas variantes genéticas pueden
surgir en él, extenderse, y reemplazar a las variantes viejas. Estos eventos suceden por
intermedio de las fuerzas microevolutivas estándar como el flujo génico, la deriva genética,
y/o la selección natural. El hecho de que las variantes génicas presentes en un linaje
evolutivo puedan ser rastreadas hasta un ancestro común significa también que los
individuos que componen este linaje deben mostrar un alto grado de relacionamiento
genético. Los mecanismos de cohesión que definen el status de especie son, por tanto,
aquellos que promueven el relacionamiento genético y que determinan las fronteras
poblacionales de la acción de las fuerzas microevolutivas.
Los conceptos de aislamiento y de reconocimiento se centran exclusivamente en el
relacionamiento genético promovido a través del intercambio de genes vía reproducción
sexual. Estas definiciones han elevado a una única fuerza microevolutiva -el flujo génico-
como criterio concluyente y exclusivo del status de especie. No hay ninguna duda de que el
flujo génico es una de las principales fuerzas microevolutivas, y por tanto los factores que
definen los límites de dispersión de las nuevas variantes génicas a través del flujo génico son
criterios válidos para el status de especie. De acuerdo con esto, la intercambiabilidad
genética se incluye en la Tabla 2 como una importante clase de mecanismos de cohesión. La
intercambiabilidad genética se refiere simplemente a la capacidad de intercambiar genes por

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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intermedio de la reproducción sexual. Esto implica un sistema de fertilización compartido en

el sentido de Paterson (1985). El intercambio efectivo de genes también exige que los
productos de la fertilización sean potencialmente viables tanto como fértiles (Templeton,
1987). Como se muestra en la Tabla 2, el rol del flujo génico en la determinación del status
de especie puede ser definido tanto en un sentido positivo (I.A en Tabla 2) como en uno
negativo (I.B en Tabla 2). Como se afirmó anteriormente, el sentido positivo provee
generalmente de una visión más certera de los procesos evolutivos involucrados en la
especiación.
El flujo génico no es la única fuerza microevolutiva que define las fronteras de un
linaje evolutivo. En realidad, la deriva genética y la selección natural juegan un rol mucho
más potente y universal debido a que estas dos clases de fuerzas microevolutivas son
aplicables a todos los organismos, no sólo a las especies sexuadas exogámicas. Una pregunta
importante es, por lo tanto, ¿qué factores definen los límites de dispersión de las nuevas
variantes génicas a través de la deriva genética y la selección natural? Dado que estas
fuerzas pueden operar en poblaciones asexuales, es obvio que los factores que limitan el
campo de acción de la deriva y la selección no son necesariamente los mismos que los que
limitan las acciones del flujo génico. Como vimos, el flujo génico requiere
intercambiabilidad genética, es decir, la capacidad de intercambiar genes durante la
reproducción sexual. Para que operen la deriva genética y la selección natural, se requiere
otro tipo de intercambiabilidad: la intercambiabilidad demográfica (Tabla 2).
Desde una perspectiva ecológica, los miembros de una población demográficamente
intercambiable comparten el mismo nicho fundamental (Hutchinson, 1965), aunque no
necesitan ser idénticos en sus capacidades de explotar ese nicho. El nicho fundamental se
define por las tolerancias intrínsecas (i.e., genéticas) de los individuos a varios factores
ambientales que determinan el rango de ambientes en los cuales los individuos son
potencialmente capaces de sobrevivir y reproducirse. El nicho realizado (Hutchinson, 1965)
se refiere al subconjunto del nicho fundamental que es efectivamente ocupado por una
especie. El nicho realizado es usualmente un subconjunto característico del nicho
fundamental debido a la falta de oportunidades de ocupar ciertas porciones del nicho
fundamental (por ejemplo, en alguna localidad los rangos ambientales pueden encontrarse
dentro de los límites de tolerancia, pero hay barreras geográficas que impiden la
colonización de dicha localidad) o debido a interacciones con otras especies que impiden la
explotación de todo el rango de tolerancia ecológica. Por tanto, el nicho realizado está
influenciado por muchos factores extrínsecos, pero la intercambiabilidad demográfica
depende solamente de las tolerancias ecológicas intrínsecas.
Mientras los individuos compartan el mismo nicho fundamental, serán
intercambiables entre ellos con respecto a los factores que controlan y regulan el crecimiento
de la población y otros atributos demográficos. Es la intercambiabilidad demográfica la que
es utilizada para definir a las poblaciones en la mayoría de los modelos de ecología de
poblaciones y de comunidades. En realidad, la mayor parte de los modelos de éstas
disciplinas ecológicas ni siquiera especifican el modo de reproducción, por lo que la
intercambiabilidad genética no es utilizada para definir una población.
Desde una perspectiva genética, las probabilidades de que una mutación neutral o
selectivamente favorable termine fijándose en una población demográficamente
intercambiable son distintas de cero sin importar el individuo particular sobre el cual ha
ocurrido la mutación. En otras palabras, cada individuo en una población demográficamente
intercambiable es un potencial ancestro común de toda la población en algún punto del
futuro. La relaciones ancestro-descendiente pueden ser tan sencillamente definidas en
poblaciones asexuales como en poblaciones sexuales. Por tanto, la intercambiabilidad

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
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demográfica no requiere de intercambiabilidad genética y es un atributo biológico distintivo

a nivel poblacional.
Así como la intercambiabilidad genética puede variar en fuerza, lo mismo puede
hacer la intercambiabilidad demográfica. Desde una perspectiva ecológica, la
intercambiabilidad demográfica completa sucede cuando todos los individuos de una
población poseen exactamente los mismos rangos y capacidades de tolerancia a todas las
variables ecológicas relevantes. La intercambiabilidad demográfica se debilita a medida que
los individuos comienzan a diferir en sus rangos o capacidades de tolerancia. Desde una
perspectiva genética, una población es completamente intercambiable demográficamente si
la probabilidad de una mutación neutral o selectivamente favorable que se dirige a la fijación
es exactamente la misma independientemente del individuo en el cual ocurra. Una población
débilmente intercambiable demográficamente consistiría de miembros que poseen
probabilidades de fijación muy diferentes (pero aún distintas de cero).
La intercambiabilidad demográfica nos permite incorporar fácilmente a otras fuerzas
microevolutivas aparte del flujo génico que son importantes en la definición de un linaje
evolutivo. Una de tales fuerzas microevolutivas es la deriva genética, que promueve la
cohesión genética a través de las relaciones ancestro-descendientes (i.e., el concepto de
idéntico por descendencia de la genética de poblaciones). Para el caso especial de los alelos
neutros (alelos que no tienen ninguna importancia selectiva), la tasa a la cual la deriva
genética promueve la identidad por descendencia depende solamente de la tasa de
mutaciones neutras y es por tanto igualmente importante en las poblaciones grandes que en
las pequeñas. Es interesante que esta predicción acerca de la tasa de evolución neutral y las
otras predicciones básicas de la teoría neutral estándar no dependan de asumir que existe
reproducción sexual -estas predicciones son igualmente aplicables a organismos asexuados.
Aunque la teoría neutral no requiere de intercambiabilidad genética, la intercambiabilidad
demográfica es una asunción crítica y necesaria (por ejemplo, Rothman y Templeton, 1980).
Haciendo solamente la asunción de que existe intercambiabilidad demográfica, es inevitable
que en algún punto en el futuro todos los alelos habrán descendido de un alelo que existe en
el presente. No hace ninguna diferencia para la operación de la deriva genética si son los
alelos o son los individuos que portan los alelos los que son intercambiables. Por tanto, la
intercambiabilidad demográfica debe ser considerada como uno de los principales
mecanismos de cohesión debido a que define los límites poblacionales para la acción de la
deriva genética. Este aspecto de la intercambiabilidad demográfica es llamado
‘reemplazabilidad’ en la Tabla 2.
La selección natural es otra fuerza poderosa que puede contribuir en la definición de
un linaje evolutivo. El concepto de selección natural no requiere de intercambiabilidad
genética debido a que los modelos de selección se formulan tan fácilmente para poblaciones
genéticamente cerradas como para las genéticamente abiertas (por ejemplo, Templeton,
1974a, 1974b). Como Darwin señaló, la selección natural requiere dos condiciones
demográficas: (1) que los organismos puedan producir más descendientes de los que son
necesarios para su estricto reemplazo, y (2) que un crecimiento poblacional ilimitado no
puede ser mantenido indefinidamente. Cuando estas condiciones demográficas son
acopladas a la variación heredable en rasgos que influyen en la supervivencia y la
reproducción, la consecuencia lógica es que los descendientes de algunos individuos
desplazarán a los de otros dentro de la población. Este aspecto de la intercambiabilidad
demográfica se denomina ‘desplazabilidad’ en la Tabla 2.
La selección natural promueve la cohesión tanto favoreciendo el relacionamiento
genético como afectando los límites de la propia intercambiabilidad demográfica. Siempre
que la selección natural cause que una nueva mutación favorable se dirija a la fijación, el
relacionamiento genético en ese locus es obviamente una consecuencia directa. Además,

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and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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mientras esta mutación se dirige a la fijación, ese subconjunto de la variación genética de la

especie que permanece ligado a la nueva mutación también se dirige a la fijación. Esto se
conoce como el efecto ‘hitchhiking’ (o genes ligados), y es importante notar que a medida
que la intercambiabilidad genética declina en importancia, los efectos del ‘hitchhiking’
aumentan su importancia, por la simple razón de que la recombinación genética es menos
efectiva para romper los estados iniciales del ligamiento que fueron creados en el momento
de la mutación. Por tanto, la fijación selectiva de un alelo por intermedio de otro es un
mecanismo de cohesión extremadamente poderoso en las poblaciones con sistemas de
reproducción genéticamente cerrados (Levin, 1981). Como ejemplo, la Figura 2 muestra los
resultados de la selección en una cepa partenogenética de D. mercatorum (Annest y
Templeton, 1978). Como puede verse en esta figura, la población convergió rápidamente a
un único genotipo para todos los loci marcadores que se examinaron. La dinámica de esta
convergencia indicó que estaban operando fuerzas selectivas muy fuertes (Annest y
Templeton, 1978). Otras réplicas de esta misma población, todas sujetas a recombinación
génica durante la primera generación partenogenética, convergieron selectivamente hacia
otros estados fenotípicos de los loci marcadores, indicando así que los loci marcadores no
estaban siendo directamente seleccionados. Por consiguiente, la selección en quizás unos
pocos loci promovió la identidad genética de todos los loci en estas poblaciones
partenogenéticas.
El grado de intercambiabilidad demográfica está íntimamente entrelazado con los
requerimientos de nicho ecológico del organismo y los hábitats que se encuentran
disponibles para satisfacer dichos requerimientos. Son estos mismos requerimientos
ecológicos y hábitats disponibles los que proveen muchas de las fuerzas selectivas que
conducen el proceso de adaptación. Por tanto, el proceso de adaptación por selección natural
puede alterar directamente los rasgos que determinan el grado de intercambiabilidad
demográfica. Las transiciones adaptativas, por lo tanto, juegan un rol directo en la definición
de los grupos de organismos demográficamente intercambiables
La importancia de las transiciones adaptativas en la definición de la
intercambiabilidad demográfica abre un grupo enteramente nuevo de mecanismos de
cohesión que restringen los cursos posibles de las transiciones adaptativas, como muestra la
Tabla 2 (II.B.2). Los primeros son las restricciones mutacionales que limitan los tipos de
variantes fenotípicas probables de ser producidas. Tales restricciones dificultan la alteración
de algunos aspectos del sistema genético y de desarrollo que existe, pero facilitan el cambio
evolutivo a lo largo de otras líneas. Por ejemplo, el género Drosophila consiste en algunas
moscas que poseen pintas, nubes o patrones pigmentados en las alas, tal como la ‘picture-
wing’ hawaiiana, y en otras que poseen alas claras, como D. melanogaster. No obstante,
como señala Basden (1984), nunca una drosophila de alas pintadas ha producido una
mutante de alas claras, ni una mutante de alas claras ha producido jamás una mutante de alas
pintadas. Este resultado negativo posee significación biológica para D. melanogaster, ya que
probablemente ningún otro eucariota superior ha sido más extensamente analizado en busca
de mutaciones visibles. Por consiguiente, Basden concluyó que a nivel de especie existe una
traba para ciertos tipos de mutaciones. Esta es simplemente otra forma de afirmar que
existen las restricciones que hacen que ciertas mutaciones sean imposibles o altamente
improbables.
Dado que se ha producido variación fenotípica por el proceso mutacional, existen
restricciones que influyen en el destino evolutivo de dicha variación (Tabla 2, II.B.2.b). En
primer lugar, hay restricciones ecológicas que seleccionan en contra a ciertos fenotipos y
que restringen el rango de variabilidad ambiental experimentada por la especie. Además,
para que una transición adaptativa persista, debe haber un nicho disponible para los
organismos con la nueva adaptación. Las restricciones ecológicas son sin lugar a dudas uno

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and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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de los mecanismos de cohesión más importantes que mantienen a las especies dentro de
grupos singámicos, como es demostrado por lo que sucede dentro de estos grupos cuando
las restricciones se alteran. Por ejemplo, bajo la mayoría de las condiciones ambientales, los
robles rojos y negros viven juntos en los mismos bosques y desarrollan polinización
cruzada. No obstante, pqermanecen como dos poblaciones distintas y cohesivas, debido a
que las bellotas híbridas de la F1 no germinan bien bajo las condiciones oscuras y frescas de
un bosque maduro. Cuando un bosque es parcialmente aclarado y raleado (principalmente
por la acción humana), las bellotas de los robles rojos y las de los robles negros germinan
mal, mientras que las bellotas híbridas lo hacen muy bien. Como resultado, muchos bosques
actuales consisten en una intergradación continua entre robles negros y rojos. Por tanto, la
cohesión normal de las poblaciones de robles rojos y negros se pierde cuando las
restricciones ecológicas son alteradas.
Las resticciones ecológicas son también importantes en los taxa asexuales debido a
que éstas restricciones a menudo determinan los límites poblacionales de la fijación
selectiva, lo cual es, como se mencionó previamente, un importante mecanismo de cohesión
en los taxa con sistemas cerrados de reproducción. Además, el trabajo de Roughgarden
(1972) predice que las poblaciones asexuales pueden desarrollar amplitudes de nichos más
nítidamente delimitadas de lo que podrían las poblaciones sexuales equivalentes. Esta
propiedad puede contribuir a explicar el hecho de que las especies asexuales sean más
fácilmente reconocibles que las especies sexuales (Holman, 1987).
Las restricciones del desarrollo constituyen la segunda clase de mecanismos de
cohesión relacionados al destino de la variación heredable en las transiciones adaptativas.
Cuando existe una fuerte selección sobre detrminado rasgo, la pleiotropía (una forma de
restricción del desarrollo) se asegura de que otros rasgos también evolucionen. Por tanto, la
pleiotropía puede facilitar los cambios evolutivos que de otra forma no ocurrirían. Aunque
muchos investigadores han puesto énfasis en la naturaleza no adaptativa, incluso mal
adaptativa, de estos cambios pleiotrópicamente inducidos, Wagner (1988) ha mostrado que
la pleiotropía es esencial para la evolución de rasgos adaptativos complejos. Examinó un
modelo en el cual la eficacia darwiniana depende de los estados simultáneos de varios rasgos
y luego contrastó modelos de evolución adaptativa en los cuales todos los rasgos eran
genéticamente independientes (no había pleiotropía ni restricciones del desarrollo) con un
modelo al cual se le imponían restricciones del desarrollo. Halló que, cuando no hay
restricciones del desarrollo, la tasa de evolución adaptativa decrece dramáticamente a
medida que aumenta el número de caracteres involucrados en la integración funcional. Por
tanto, las restricciones del desarrollo y la pleiotropía parecen ser necesarias para la evolución
de fenotipos funcionalmente integrados.
Aún más evolución adaptativa puede ser facilitada incluso cuando la adaptación
primaria induce efectos pleiotrópicos que son no adaptativos. Este fenómeno puede ser
ilustrado por las adaptaciones a la malaria en humanos (Templeton, 1982). Las adaptaciones
primarias a la malaria (tales como la condición falciforme) a menudo inducen efectos
pleiotrópicos altamente deletéreos (como la anemia), los cuales, a su vez, generan procesos
adaptativos secundarios en modificadores para disminuir o eliminar los efectos deletéreos
(tales como la persistencia de la hemoglobina fetal para suprimir la anemia). De esta forma
una sóla transición adaptativa puede disparar una cascada de transiciones secundarias, las
cuales se acumulan y pueden tener un gran impacto en la intercambiabilidad demográfica.
Otro mecanismo de cohesión que restringe el destino evolutivo de la variabilidad
fenotípica es la restricción histórica. La evolución es un proceso histórico y, en
consecuencia, el potencial evolutivo de un linaje está modelado por sus transiciones
adaptativas pasadas. Por ejemplo; un prerequisito para la evolución de la coloración
aposemática en insectos con larvas gregarias es la evolución de la mala palatabilidad. Sin la

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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existencia previa del sabor desagradable, no hay fuerza selectiva a favor de la coloración de
advertencia dentro de la progenie (Templeton, 1979). Por tanto, la adaptación del mal sabor
es una restricción histórica para la evolución de la coloración aposemática y las larvas
gregarias. Esta predicción fue puesta a prueba recientemente por Sillen-Tullberg (1988),
quien mostró a través de un análisis filogenético que en todos los casos en los que la
resolución era posible, el mal sabor evolucionó previamente a la evolución de larvas
gregarias y aposemáticas. Como muestra este ejemplo, una adaptación puede hacer que una
segunda sea más probable, reforzando así la cohesión del linaje que comparte estas
transiciones adaptativas.
Las restricciones de la genética de poblaciones también limitan el destino evolutivo
de la nueva variabilidad fenotípica. Estas restricciones emergen de la interacción de la
estructura poblacional (sistema de apareamiento, tamaño poblacional, subdivisión
poblacional) con la arquitectura genética subyacente a los rasgos seleccionados (la relación
genotipo-fenotipo, número de loci, relaciones de ligamiento, etc.). Por ejemplo, en 1924
Haldane mostró que los genes dominantes selectivamente favorecidos son mucho más
probables de ser fijados que los genes recesivos selectivamente favorecidos en las
poblaciones con apareamientos al azar. Sin embargo, esta restricción desaparece si el
sistema de apareamiento cambia desde apareamientos al azar hacia la endogamia
(Templeton, 1982). De este modo, una alteración del sistema de apareamiento puede alterar
la cohesión genética y fenotípica de una población haciendo que clases enteras de
variabilidad genética nueva respondan a la selección natural.

VENTAJAS DEL CONCEPTO COHESIVO DE ESPECIE

El concepto cohesivo de especie define a la especie como linaje evolutivo a través de

los mecanismos que limitan las fronteras poblacionales de la acción de las fuerzas
microevolutivas básicas como el flujo génico, la selección natural y la deriva genética. La
esencia genética de un linaje evolutivo es que una nueva mutación puede dirigirse a la
fijación dentro del mismo; y la deriva genética así como el flujo génico son fuerzas
poderosas que pueden causar tales fijaciones. Por tanto, no existe ninguna buena razón por la
cual el flujo génico deba ser el único mecanismo microevolutivo utilizado para definir un
linaje evolutivo; no obstante esto es precisamente lo que hacen los conceptos de aislamiento
y de reconocimiento.
Bajo el concepto de cohesión, muchos mecanismos de cohesión con base genética
(Tabla 2) pueden jugar un rol en la definición de una especie. No todas las especies serán
mantenidas por los mismos mecanismos de cohesión o por las mismas combinaciones de
mecanismos de cohesión, tal como los partidarios del concepto de aislamiento reconocen
que no todos los mecanismos de aislamiento son igualmente importantes en todos los casos.
Ajustando la combinación de mecanismos de cohesión, es posible tener en cuenta bajo un
único concepto de especie a los taxa asexuales, a los taxa que caen dentro del dominio de los
conceptos de aislamiento y de reconocimiento, y a los miembros de grupos singámicos.
La Figura 3 ofrece una representación gráfica simpificada de la importancia relativa
en la definición de especie de la intercambiabilidad genética versus la demográfica sobre el
contínuo reproductivo completo. Para taxa asexuales, la intercambiabilidad genética no es
relevante, y el status de especie se determina exclusivamente por la intercambiabilidad
demográfica. A medida que el sistema reproductivo se vuelve más abierto, la
intercambiabilidad genética no sólo se convierte en un factor, sino que la intercambiabilidad
demográfica disminuye en importancia debido a que el reemplazo selectivo se vuelve cada
vez menos efectivo en promover el relacionamiento genético. En un rango intermedio,

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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domina la intercambiabilidad genética porque los factores que determinan los límites del
flujo génico también limitan la acción de la deriva y la selección en las poblaciones
mendelianas exogámicas. En este dominio, los conceptos de aislamiento y de
reconocimiento son válidos, y por tanto, ambos constituyen casos especiales del concepto
cohesivo más general de especie. Finalmente, si nos movemos hacia el extremo del contínuo
de los grupos singámicos, decrece la importancia de la intercambiabilidad genética en
relación a las restricciones ecológicas que definen la intercambiabilidad demográfica.
Esta continuidad en la aplicación del concepto de cohesión es consistente con la
realidad biológica de que existe un continuo en el grado de apertura genética de los sistemas
de reproducción que se encuentran en el mundo orgánico. Esta es una ventaja tremenda
sobre los conceptos de aislamiento y de reconocimiento que son aplicables sólo al rango
medio de este continuo reproductivo y que tratan con el resto del rango o bien negando la
existencia de especies fuera de este rango (por ejemplo, Vrba, 1985) o utilizando conceptos
de especies cualitativamente distintos (por ejemplo, Mayr, 1970) para imponerle al continuo
reproductivo un carácter discreto artificial.
Otro punto fuerte del concepto de cohesión es que clarifica lo que se quiere decir con
una ‘buena especie’ y la naturaleza de las dificultades que pueden ocurrir con los conceptos
de aislamiento y de reconocimiento. Las ‘buenas especies’ son consideradas generalmente
como taxa geográficamente cohesivos que pueden coexistir por largos períodos de tiempo
sin ninguna ruptura en su integridad genética. El hecho de que no haya ruptura en la
integridad genética a pesar de la simpatría implica la falta de intercambiabilidad genética
entre los taxa. Sin embargo, la condición de coexistencia prolongada también implica que
poseen nichos ecológicos diferentes (Mayr, 1970). Luego, las ‘buenas especies’ son aquellas
que se encuentran bien definidas tanto por la intercambiabilidad genética como por la
demográfica. (En forma similar, los miembros de un taxón superior ‘bueno’ carecen tanto de
intercambiabilidad genética como demográfica.) Dada esta definición de ‘buena especie’,
hay dos maneras principales de desviarse de este ideal. Una sucede cuando las fronteras
poblacionales definidas por la intercambiabilidad genética son más estrechas que las
definidas por la intercambiabilidad demográfica. Este es precisamente el problema de los
taxa asexuales previamente discutido. La otra forma de desviación sucede cuando las
fronteras definidas por la intercambiabilidad genética son mayores que las definidas por la
intercambiabilidad demográfica -en otras palabras, el problema propuesto por las especies
singámicas. Por tanto, estos dos problemas aparentemente tan dispares bajo los conceptos de
aislamiento y de reconocimiento poseen de hecho un causa subyacente común: las fronteras
definidas por la intercambiabilidad demográfica son diferentes de las definidas por la
intercambiabilidad genética.
La especiación es generalmente un proceso, no un evento (Templeton, 1981).
Mientras el proceso esté ocurriendo, la tendencia es a tener ‘malas’ especies. Aunque los
taxa asociados con este proceso incompleto de especiación son la perdición para el
taxónomo, proveen la mejor visión dentro de la especiación. Al proveer una definición
precisa de ‘mala especie’ (el conflicto entre la intercambiabilidad genética y la
demográfica), el concepto de cohesión es una herramienta útil para obtener una visión
profunda dentro del proceso de especiación. Las ‘malas especies’ ya no deben ser
consideradas como un diverso grupo de casos especiales; más bien, el concepto de cohesión
provee los medios para ver los patrones observados en estos taxa problemáticos. Por
ejemplo, Levene (1953) postuló un modelo hace mucho tiempo en el cual diferentes
genotipos desarrollaban diferentes eficacias darwinianas en nichos demográficamente
independientes. Sin embargo, en este modelo, hay intercambiabilidad genética completa y
aún hay suficiente intercambiabilidad demográfica entre todos los genotipos dentro de los
varios nichos realizados (a través del desplazamiento selectivo dentro del nicho) que se trata

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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Lecturas traducidas. Laboratorio de Evolución, Facultad de Ciencias ______________________________________ 16

claramente de un modelo de polimorfismo intraespecífico. La situación modelada por

Levene (1953) porta ciertas semejanzas con los ejemplos de los grupos singámicos
discutidos anteriormente en que surge un conflicto entre la intercambiabilidad genética y la
demográfica (a través de la adaptación a diferentes nichos ecológicos realizados que alteran
las tolerancias intrínsecas que definen al nicho fundamental). Por tanto, puede haber un
continuo de fuerza relativa entre estos conflictivos criterios de fronteras entre las especies.
Es interesante el hecho de que ha habido un reconocimiento implícito de esta tensión en la
literatura de la especiación. La mayor parte de los modelos de especiación simpátrida
comienzan con un modelo del tipo de Levene, siendo el modelo de Wilson (en este
volumen) un ejemplo de ello (ver también Maynard Smith, 1966). Aunque estos modelos en
detalle difieren en gran medida, el concepto de cohesión clarifica el significado evolutivo de
esta clase entera de modelos de especiación: es la evolución de la no-intercambiabilidad
demográfica lo que dispara en estos casos el proceso de especiación, y la especiación
procede a través de los cambios en la importancia relativa de la intercambiabilidad genética
y demográfica dentro y entre las poblaciones mientras se adaptan a diferentes nichos
realizados. De este modo, de un grupo aparentemente diverso de modelos de especiación
todos poseen un tema en común, y el concepto de cohesión permite discernir claramente este
tema.
Nótese también que la selección natural es la fuerza que dirige la especiación en
todos estos modelos de especiación simpátrida, siendo secundarios los efectos del flujo
génico. Debido a que el concepto de cohesión incorpora explícitamente a un amplio grupo
de fuerzas microevolutivas como importantes en la especiación, podemos tratar directamente
a la selección natural como si fuera en estos modelos el disparador primario de la
especiación en vez de tener que explicar constantemente el significado evolutivo de la
selección natural en términos de sus efectos secundarios sobre el flujo génico. El concepto
de cohesión por lo tanto facilita el estudio de la especiación como un proceso evolutivo
volviendo explícito el rol jugado por una amplia muestra de fuerzas evolutivas que incluyen
al flujo génico, pero que no están limitadas al mismo.
Como ilustran los modelos de especiación del tipo de Levene, una de las fuerzas
evolutivas importantes en la especiación es la selección natural. La selección natural es
importante para la definición de especie bajo el concepto de cohesión en parte debido al
impacto de las transiciones adaptativas en la intercambiabilidad demográfica. Es interesante
que Mayr (1970) argumenta que la mayoría de las especies poseen nichos ecológicos
distintivos (es decir, que no son demográficamente intercambiables) y que esta diferencia
ecológica es la ‘piedra angular de la evolución’ porque sirve como base de la diversificación
del mundo orgánico, de la radiación adaptativa, y del progreso evolutivo. Si bien Mayr
concluye por lo tanto que ‘el significado evolutivo de especie’ yace en su distinción
ecológica, aún argumenta que las transiciones adaptativas y la selección natural no juegan en
general un rol directo en la especiación y contribuyen a definir una especie sólo a través del
‘producto secundario incidental’ que constituyen los mecanismos de aislamiento. Mayr
permite que las presiones selectivas refuercen los mecanismos de aislamiento y acentúen la
exclusión ecológica si se ha establecido la simpatría, pero pone énfasis en que esto ocurre
sólo luego de que el proceso de especiación ha sido básicamente completado. Por tanto, bajo
el concepto de aislamiento, los factores responsables del ‘significado evolutivo de especie’
no juegan un rol directo en la definición de especie. Bajo el concepto de cohesión, el
significado evolutivo de una especie puede surgir directamente de los atributos que la
definen.

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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Lecturas traducidas. Laboratorio de Evolución, Facultad de Ciencias ______________________________________ 17

ESPECIACIÓN

Ahora que la especie ha sido definida, ¿qué es la especiación? La especiación es el

proceso por el cual nuevos sistemas genéticos de mecanismos de cohesión evolucionan
dentro de una población. Este proceso puede considerarse análogo al proceso de asimilación
genética de los fenotipos individuales. La asimilación genética es un proceso discutido por
Waddington (1957) a la luz de su trabajo con la mosca de la fruta, Drosophila melanogaster.
Por ejemplo, descubrió que sometiendo algunas cepas de esta mosca a choques térmicos,
muchas de las moscas expresarían un fenotipo en el cual se observa la falta de cierta vena de
las alas. Inicialmente, este fenotipo ‘crossveinless’ parecía ser puramente ambiental.
Seleccionando artificialmente a las moscas que expresaban el fenotipo, Waddington
descubrió que estaba seleccionando también a la predisposición genética para expresar este
fenotipo. Por lo tanto, luego de varias generaciones este fenotipo ‘ambiental’ adquirió una
base genética hasta tal punto que eventualmente comenzó a expresarse aún en ausencia del
choque térmico. En forma similar, una alteración puramente ambiental en la manifestación
de la cohesión puede conducir a condiciones evolutivas que favorecen la asimilación del
nuevo patrón de cohesión dentro del pool génico. Por ejemplo, considérese el caso de la
especiacción alopátrida en el cual un taxa ancestral que se encontraba distribuido en forma
continua en una región es luego dividido, por la erección de alguna barrera geográfica, en
dos subpoblaciones totalmente aisladas. La erección de la barrera geográfica altera
potencialmente la manifestación de varios mecanismos de cohesión. Para taxa sexuados, se
altera el relacionamiento genético a través del flujo génico, y para taxa tanto sexuados como
asexuados, el potencial para el relacionamiento genético a través de la deriva génica y la
selección natural se altera tan pronto como las poblaciones se vuelven demográficamente
independientes debido a la separación geográfica. Además, si la barrera geográfica se asocia
con la alteración ambiental o con la alteración de los sistemas de apareamiento, las
alteraciones en las restricciones de las transiciones adaptativas pueden ser directamente
inducidas y un nuevo nicho realizado puede ser ocupado. Sin embargo, nada de esto
constituye la especiación hasta que estas alteraciones en la manifestación de la
intercambiabilidad genética y demográfica son genéticamente asimiladas dentro del pool
génico como nuevos mecanismos de cohesión. Por consiguiente, la especiación es la
asimilación genética de patrones alterados de intercambiabilidad genética y demográfica
dentro de los mecanismos intrínsecos de cohesión.
Esta es una definición simple de la especiación, pero debido a la amplitud del
concepto cohesivo de especie, esta definición puede utilizarse para estudiar una gran
variedad de procesos evolutivos que contribuyen a la formación de una nueva especie dentro
de un mismo marco mecanístico. Esta es una perspectiva excitante, y espero que resulte en
una aplicación más profunda de la genética evolutiva al problema del origen de las especies.

RESUMEN

El ‘concepto biológico de especie’ define a las especies como comunidades

reproductivas que están separadas de otras comunidades similares por barreras intrínsecas de
aislamiento. Sin embargo, existen otros conceptos ‘biológicos’ de especie, por lo cual el
concepto biológico clásico de especie se describe mejor como el concepto de especie ‘por
aislamiento’. El propósito de este capítulo era proveer una definición biológica de especie
que provenga directamente de los mecanismos evolutivos responsables de la especiación y
sus consecuencias genéticas.

Templeton, A.. 1989.The meaning of species and speciation: a genetic perspective. En Speciation
and its consequenes editado por D. Otte y J. Endler. Sianuer, Sunderland
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Lecturas traducidas. Laboratorio de Evolución, Facultad de Ciencias ______________________________________ 18

Los puntos fuertes y débiles de los conceptos evolutivo, de aislamiento y de

reconocimiento fueron revisados y los tres fueros juzgados como inadecuados para este
propósito. Como alternativa, propuse el concepto cohesivo que define a la especie como el
grupo más inclusivo de organismos que poseen el potencial para la intercambiabilidad
genética y demográfica. Este concepto toma ideas prestadas de los tres conceptos biológicos
de especie. A diferencia de los conceptos de aislamiento y de reconocimiento, es aplicable a
todo el continuo de sistemas reproductivos observados en el mundo orgánico. A diferencia
del concepto evolutivo, identifica mecanismos específicos que dirigen el proceso evolutivo
de la especiación. El concepto cohesivo facilita el estudio de la especiación a la vez que es
compatible con las consecuencias genéticas de dicho proceso.

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 SEMINARIO II: MECANISMOS DE AISLAMIENTO Y  
MODELOS DE ESPECIACIÓN 
Marcela Rodriguero & Abel Carcagno 
 

En  este  seminario  se  analizarán  dos  modelos  de  especiación  vinculados  a  distintos 
Mecanismos  de  Aislamiento  Reproductivo  (MARs)  por  medio  de  la  discusión  de  dos  casos 
particulares: el modelo de especiación infecciosa y el modelo de especiación simpátrica. 
 
Preguntas Introductorias 
1‐ ¿Qué son los Mecanismos de Aislamiento Reproductivo (MARs) y qué concepto de especie 
los contempla? Clasifíquelos y de ejemplos. 
2‐  ¿Cuál  es  la  clasificación  de  los  procesos  especiogénicos  de  acuerdo  con  la  escala 
geográfica en la que se producen? 
 
Modelo I: Especiación infecciosa 
• Wade M.J. (2001) Infectious speciation. Nature 409: 675‐677. 
•  Bordenstein  S.R.,  O’Hara  F.P.  &  Werren  J.H.  (2001)  Wolbachia  –  induced  incompatibility 
precedes other Irbid incompatibilities in Nasonia. Nature 409: 707‐ 710. 
 
3‐ ¿La especiación infecciosa es un evento especiogénico dirigido por el hospedador o por el 
parásito? ¿Cuáles serían las implicancias evolutivas de cada caso? 
4‐  ¿Considera  que  la  incompatibilidad  citoplasmática  unidireccional  podría  conducir  al 
aislamiento reproductivo? 
5‐ ¿Cuáles son las diferencias entre el modelo génico y el infeccioso planteado en la figura 2 
del trabajo de Wade? 
6‐  ¿Cuáles  son  las  hipótesis  de  trabajo  de  Bordenstein  y  colaboradores?  Exprese  su 
respuesta en términos de hipótesis nula y alternativa. 
7‐ ¿Qué concepto de especie las sustentan? 
8‐ Analice la figura 1. A partir de estos resultados obtenidos ¿es posible refutar la hipótesis 
nula? 
9‐ ¿Qué aproximaciones experimentales utilizaron posteriormente los autores para sostener 
su  argumento?  ¿Qué  tipos  de  MARs  analizaron  a  través  de  ellas  y  cómo  incidieron  los 
resultados en las hipótesis de trabajo (i.e. nula y altenativa)? 
10‐ ¿Qué crítica podría realizar al sistema bajo estudio? 

77
Modelo II: Especiación simpátrica 
• Linn C., Feder J.L., Nojima S., Dambroski S.H., Berlocher S.H. & Roelofs W (2003) Fruit odor 
discrimination and sypatric host formaion in Rhagoletis. PNAS 100: 11490‐11493. 
 
11‐  ¿Cuáles  son  los  rasgos  de  Rhagoletis  pomonella  que  la  señalan  como  una  especie 
adecuada para el estudio de la especiación simpátrica? 
12‐ Desde el punto de vista aislacionista propugnado por Mayr y Dobzhansky ¿qué tipo de 
MARs  esperaría  que  tuvieran  mayor  incidencia  en  la  especiación  simpátrica?  Señale  los 
supuestos del modelo. 
13‐  ¿Qué  tipo  de  estímulo  podrían  utilizar  las  razas  de  R.  pomonella  para  distinguir  a  su 
hospedador? Vincule esta respuesta a los supuestos enunciados anteriormente. 
14‐  Analice  cuidadosamente  la  figura  1.  ¿Qué  conclusión  extrae  ante  cada  estímulo 
presentado a las razas bajo estudio? 
15‐  ¿Existe  consenso  entre  los  resultados  obtenidos  bajo  condiciones  de  laboratorio  y  los 
obtenidos a partir de condiciones naturales? 
16‐  ¿La  capacidad  de  discriminación  de  la  especie  hospedadora  por  parte  de  la  raza  de  la 
manzana sería una característica derivada o primitiva? ¿Cómo arribaron los investigadores a 
este resultado? 
 
Preguntas unificadoras 
17‐  ¿Cómo  describiría  un  modelo  de  especiación  por  aislamiento  geográfico?  Suponiendo 
que antes de completarse el aislamiento reproductivo se restableciera el flujo génico y que 
los grupos previamente aislados produjeran una F1... ¿qué ocurriría si esa F1 tuviera menor 
fitness  que  ambos  parentales?  ¿Qué  pasaría  si  esa  F1  tuviera  mayor  fitness  que  sus 
parentales? 
18‐ ¿Considera posible revertir la aparición de los MARs? ¿Por qué? 
 

78
Coyne, J. A. & Orr, H. A. 2004. Speciation. Sinauer, Sunderland, MA. Clasificación
de los mecanismos de aislamiento reproductivo (MARs)

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Ridley, M. 2004. Evolution. 3rd Edition. Blackwell Publishing. Malden, MA.

382 PART 4 / Evolution and Diversity

14.1 How can one species split into two reproductively

isolated groups of organisms?

Reproductive isolation is the main The crucial event for the origin of a new species is reproductive isolation. As we saw in
topic in research on speciation Chapter 13, the members of a species usually differ genetically, ecologically, and in their
behavior and morphology (that is, phenetically) from other species, as well as in who
they will interbreed with. Some biologists prefer to define species not by reproductive
isolation but by other properties, such as genetic or ecological differences. Probably no
single property can provide a universal species definition, applicable to all animals,
plants, and microorganisms. However, many species do differ by being reproductively
isolated, and even if the evolution of reproductive isolation is not always the crucial
event in speciation, it is certainly the key event in research on speciation. The topic of
this chapter is the evolution of reproductive isolation. The aim is to understand how a
barrier to interbreeding can evolve between two populations, such that one species
evolves into two.
Reproductive isolation can be caused by many features of organisms (see Table 13.1,
p. 356). However, for most of the research in this chapter, we only need a distinction
between prezygotic and postzygotic isolation. Prezygotic isolation exists when, for
instance, two species have different courtship or mate choices, or different breeding
seasons. Postzygotic isolation exists when two species do interbreed, but their hybrid
offspring have low viability or fertility. Some of the theories of speciation apply only to
prezygotic isolation, some only to postzygotic isolation, and some to both.

14.2 A newly evolving species could theoretically have an

allopatric, parapatric, or sympatric geographic relation
with its ancestor

We can start with a distinction between different geographic conditions in the speciat-
ing populations. If a new species evolves in geographic isolation from its ancestor, the
Speciating populations can have process is called allopatric speciation. If the new species evolves in a geographically con-
various kinds of geographic tiguous population, it is called parapatric speciation. If the new species evolves within
relations the geographic range of its ancestor, it is called sympatric speciation (Figure 14.1). The
distinctions between these three kinds of speciation can blur, but we shall begin the
chapter with the most important of the three processes: allopatric speciation. Almost
all biologists accept that allopatric speciation occurs. The importance of parapatric and
sympatric speciation are more in doubt, and we shall come on to them later.
In allopatric speciation, new species evolve when one (or more) population of a
species becomes separated from the other populations of the species, in the manner of
Figure 14.1a. This kind of event often happens in nature. For example, a species could
split into two separate populations if a physical barrier divided its geographic range.
The barrier could be something like a new mountain range, or river, cutting through
the formerly continuous population. Or the intermediate populations of a species
may be driven extinct, perhaps by a local disease outbreak, leaving the geographically

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 CHAPTER 14 / Speciation 383

(a)
Space

Time

(b)

Figure 14.1
Three main theoretical types of speciation can be distinguished
according to the geographic relations of the ancestral species
(c) and the newly evolving species. (a) In allopatric speciation the
new species forms geographically apart from its ancestor;
(b) in parapatric speciation the new species forms in a contiguous
population; and (c) in sympatric speciation a new species emerges
from within the geographic range of its ancestor.

extreme populations cut off from each other. Or a subpopulation may migrate (actively
or passively) to a new place, outside the range of the ancestral species, such as when a
few individuals colonize an island away from the mainland. Such a population, at the
edge of the main range of a species, is called a “peripheral isolate.”
Geographic separation alone is not One way or another, a species can become geographically subdivided, consisting of a
reproductive isolation number of populations between which gene flow has been cut off. This is not, in itself,
an isolating barrier in the sense of Table 13.1 (p. 356). An isolating barrier is an evolved
property of a species that prevents interbreeding. When two populations are geograph-
ically cut off, gene flow ceases but only because members of the population do not
meet. The two populations have not yet evolved a genetic difference. The evolution of
an isolating barrier requires some new character, such as a new courtship song, to
evolve in at least one of the populations a a new character that has the effect of prevent-
ing gene flow. In the theory of allopatric speciation, the cessation of gene flow between
allopatric populations leads, over time, to the evolution of intrinsic isolating barriers
between the populations. Let us see what happens to the reproductive isolation
between these populations over evolutionary time.

14.3 Reproductive isolation can evolve as a by-product of

divergence in allopatric populations

We have two main kinds of evidence that reproductive isolation evolves when
geographically separate populations are evolving apart. One comes from laboratory
experiments and the other comes from biogeographic observations.

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populations. Within one population, natural selection will not favor a genetic change
that is incompatible with genes at other loci.
Prezygotic isolation, however, does not require incompatible genetic change at sev-
eral loci. Prezygotic isolation can evolve as a by-product of divergence if the characters
that have diverged between populations are genetically correlated with characters caus-
ing prezygotic isolation. This theory is less strongly tied to the theory of allopatric spe-
ciation. The process can indeed occur between populations that are separately evolving
in different places. But adaptive divergence can also occur within one population, as we
shall see, and that at least raises the possibility that speciation could occur non-
allopatrically.
Reinforcement works in sympatry The other theory was reinforcement. Reinforcement only occurs in sympatry.
Natural selection only favors discrimination among potential mates for the range of
mates that are present in a particular place. The theory of reinforcement is only weakly
tied to the theory of allopatric speciation. Indeed, it is hardly an allopatric theory of
speciation at all. Reinforcement was only used in the allopatric theory to “finish off ”
speciation that was incomplete in allopatry.
Thus, in the theories we have met so far, speciation in non-allopatric populations
is relatively unlikely. One well supported theory, the Dobzhansky–Muller theory, is
allopatric. Reinforcement is a sympatric process, but (as we saw) little supported by
evidence and problematic in theory. However, non-allopatric speciation has not been
ruled out, and in the next two sections we shall look some more at whether speciation
could occur parapatrically or sympatrically.

14.9 Parapatric speciation

14.9.1 Parapatric speciation begins with the evolution of a

stepped cline
In parapatric speciation, the new species evolve from contiguous populations, rather
than completely separate ones, as in allopatric speciation (see Figure 14.1). The full
process could occur as follows. Initially, one species is distributed in space. The species
evolves a “stepped cline” pattern of geographic variation (Section 13.4.3, p. 363). The
stepped cline could exist because of an abrupt environmental change: one form of the
species would be adapted to the conditions on one side of the boundary, the other form
to the conditions on the other side of the boundary.
A hybrid zone is a stepped cline in which the forms on either side of the boundary are
sufficiently different that they can easily be recognized. The two forms may have been
given different taxonomic names, as subspecies or races, or they may be different
enough to have been classified as separate species.
European crows provide an The carrion crow (Corvus corone) and hooded crow (C. cornix) in Europe are a
example of a hybrid zone classic example of species round a hybrid zone (Figure 14.13). The hooded crow is
distributed more to the east, the carrion crow to the west, with the two species meet-
ing along a line in central Europe. At that line a the hybrid zone a they interbreed and
produce hybrids. The hybrid zone for the crows was first recognized phenotypically,

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C. cornix
C. corone

Figure 14.13
Hybrid zone between the carrion crow (Cornix corone) and
hooded crow (C. cornix) in Europe. Here the two crows are
shown as two separate species, but some taxonomists classify
them as subspecies. Redrawn, by permission of the publisher,
from Mayr (1963). © 1963 President and Fellows of Harvard
College.

because the hooded crow is gray with a black head and tail, whereas the carrion crow is
black all over. The two species (or near species) are now known to differ in many other
respects too. The fact that the crows interbreed in the hybrid zone means that speci-
ation between them is incomplete. We shall meet some more examples of hybrid zones
in Section 17.4 (p. 497).
The conditions in a hybrid zone (or a stepped cline) are particularly ripe for
Many hybrid zones are tension speciation if it is a tension zone. A tension zone exists when the hybrids between the
zones . . . forms on either side of the boundary are selectively disadvantageous. (A hybrid zone
is not a tension zone if the hybrids have intermediate, or superior, fitness to the
pure forms.) For instance, if one homozygote (AA) is adapted to one environment,
and another homozygote (aa) to another environment, heterozygotes (Aa) will be
produced where the two environments meet up. If the heterozygotes are disadvant-
ageous, the meeting place is an example of a tension zone. Most known hybrid zones
are in fact tension zones (see, for example, Barton & Hewitt’s (1985) review of
170 hybrid zones).
. . . in which reinforcement may In a tension zone, the conditions are exactly the preconditions for reinforcement
operate (Section 14.6.1). Matings within a type are advantageous, and matings between types
produce disadvantageous hybrids. Natural selection favors assortative mating. We can
therefore imagine a sequence where a stepped cline initially evolves, and then becomes
distinct enough to count as a hybrid zone. We are near the border of the origin of a new
species. Reinforcement could then finish speciation off, eliminating hybridization
from the hybrid zone. That sequence of events constitutes parapatric speciation.
The strong point of the theory of parapatric speciation is that the environment
“stabilizes” the preconditions for reinforcement. We saw that these conditions are
liable to autodestruct, as the two forms interbreed, or as one eliminates the other. But
if the environment varies in space, the clinal variation will be maintained. Parapatric
speciation could work, in theory.

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 CHAPTER 14 / Speciation 411

14.9.2 Evidence for the theory of parapatric speciation is

relatively weak
The theory of parapatric speciation has two main weak points in the evidence. One is
the evolutionary history of hybrid zones. Hybrid zones can be “primary” or “sec-
ondary.” A hybrid zone is primary if it evolved while the species had approximately
Most hybrid zones are due to their current geographic distribution. It is secondary if in the past the species was sub-
secondary contact divided into separate populations, where the differences between the forms evolved,
and the populations later expanded and met up at what is now the hybrid zone. Real
hybrid zones only illustrate a stage in parapatric speciation if they are primary. The
abundance of hybrid zones in nature would only be evidence that parapatric speciation
is a plausible process if those hybrid zones are mainly primary. If most hybrid zones are
secondary, the difference between the forms evolved allopatrically not parapatrically.
In fact the evidence suggests that most hybrid zones are secondary. Hooded and carrion
crows, for instance, have met up after their ranges expanded following the most recent
ice age. Indeed, range expansion following the ice age is a common explanation of
hybrid zones (Section 17.4, p. 497). Hybrid zones provide little support for the theory
of parapatric speciation.
Secondly, if reinforcement operates in hybrid zones, we predict that prezygotic
isolation will be stronger in the hybrid zone than between the two forms away from
the hybrid zone. The prediction is a special case of the general biogeographic test of
reinforcement (Section 14.6.3). The evidence does not support the prediction: we have
little good evidence that prezygotic isolation is reinforced in hybrid zones.
Thus, the process of parapatric speciation is possible in theory. The theory solves one
key problem in reinforcement. Most (but not all) stages of parapatric speciation can be
illustrated by evidence. But parapatric speciation lacks the solid weight of supporting
evidence and the theoretical near inevitability of allopatric speciation. Parapatric specia-
tion cannot be ruled out, and probably operates in some cases. But the case that it is
important has still to be made.

14.10 Sympatric speciation

14.10.1 Sympatric speciation is theoretically possible

In sympatric speciation, a species splits into two without any separation of the ancestral
species’ geographic range (see Figure 14.1). Sympatric speciation has been a source of
recurrent controversy for a century or so. Mayr (1942, 1963) particularly cast doubt on
it, and in doing so has stimulated others to look for evidence and to work out the theor-
etical conditions under which it may be possible.
In the theory of parapatric speciation, the initial stage in speciation is a spatial
polymorphism (or stepped cline). In sympatric speciation, the initial stage is a poly-
morphism that does not depend on space within a population. For instance, two forms
of a species may be adapted to eat different foods. If matings between the two are dis-
advantageous, because hybrids have low fitness, reinforcement will operate between

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them. Most models of sympatric speciation suppose that natural selection initially
establishes a polymorphism, and then selection favors prezygotic isolation between
the polymorphic forms. “Host shifts” in a fly called Rhagoletis pomonella provide a case
study that may illustrate part of the process.

14.10.2 Phytophagous insects may split sympatrically by host shifts

The apple maggot fly has only Rhagoletis pomonella is a tephritid fly and a pest of apples. It lays its eggs in apples
recently moved on to apples and the maggot then ruins the fruit, but this was not always so. In North America,
R. pomonella’s native larval resource is the hawthorn. Only in 1864 were these species
first found on apples. Since then it has expanded through the orchards of North
America, and has also started to exploit cherries, pears, and roses. These moves to new
food plants are called host shifts. In the host shift of R. pomonella, speciation may be
happening before our eyes.
The R. pomonella on the different hosts are currently different genetic races. Females
prefer to lay their eggs in the kind of fruit they grew up in: females isolated as they
emerge from apples will later choose to lay eggs in apples, given a choice in the labor-
atory. Likewise, adult males tend to wait on the host species that they grew up in, and
mating takes place on the fruit before the females oviposit. Thus there is assortative
mating: male flies from apples mate with females from apples, males from hawthorn
with females from hawthorn.
The races on apples show some The races are presumably about 140 generations old (given that they first moved on
isolation from the ancestral races to apples nearly one and a half centuries ago). Is this long enough for genetic differences
on hawthorn between the races to have built up? Gel electrophoresis shows that the two races have
evolved extensive differences in their enzymes. They also differ genetically in their
development time: maggots in apples develop in about 40 days, whereas hawthorn
maggots develop in 55–60 days. This difference also acts to increase the reproductive
isolation between the races, because the adults of the two races are not active at the
same time.
Apples and hawthorns differ and selection will therefore probably favor different
characters in each race; this may be the reason for their divergence. If it is, selection may
also favor prezygotic isolation and speciation. If flies from the different races are put
together in the lab, however, they mate together indiscriminately. Either reinforcement
has not operated when it might have been expected, or, alternatively, the differences in
behavior and development time in the field may be enough to reduce interbreeding
to the level natural selection favors. Selection would then not be acting to reinforce
the degree of prezygotic isolation. We do not know which interpretation is correct;
we need to know more about the forces maintaining the genetic differences between
the races. Once again, the evidence for reinforcement is the weak point in a theory of
speciation.
But the example is incomplete In the case of host shifts, we can be practically certain that the initial host shift, and
formation of a new race, has happened in sympatry. The shift took place in historic
time. However, it is not a full example of sympatric speciation because the races have
not fully speciated. Indeed, we do not know whether they will, or whether the current
situation, with incomplete speciation, is stable.

85

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 news and views
the relative production of thorium to urani- to find more examples of such stars, as our
um because these elements are separated by surveys of the Galactic halo with the new
only two atomic numbers. And the different generation of very large telescopes is just
decay rates of 232Th and 238U ensure that the beginning. With new discoveries, more age
abundance ratio of these two elements will estimates will be found, further nailing down
be a sensitive function of their age. Cayrel et the exact age of the Universe. ■
al.1 propose that the neutron-capture mat- Christopher Sneden is in the Department of
erial in the atmosphere of CS31082-001 has Astronomy, University of Texas at Austin, Austin, 100 YEARS AGO
an age of 12.5 Gyr with an uncertainty of 3.3 Texas 78712, USA. Dr. R. A. Daly, of the Department of Geology
Gyr, a more accurate estimate of the age of e-mail: chris@verdi.as.utexas.edu and Geography of Harvard University, is
the Universe. Further analysis of the whole 1. Cayrel, R. et al. Nature 409, 691–692 (2001). endeavouring to organise a geological and
range of neutron-capture elements in this 2. Chaboyer, B. Phys. Rep. 307, 23–30 (1998). geographical excursion in the North Atlantic
3. Beers, T. C., Preston, G. W. & Schectman, S. Astron. J. 103,
star will refine this age estimate, narrowing 1987–2034 (1992).
for the summer of 1901. Conditionally on the
the uncertainty. 4. Butcher, H. R. Nature 328, 127–131 (1987). formation of a sufficiently large party, a
We now know of a handful of stars born 5. Sneden, C. et al. Astrophys. J. 533, L139–L142 (2000). steamer of about 1000 tons, specially
6. Westin, J., Sneden, C., Gustafsson, B. & Cowan, J. J. Astrophys. J.
early in our Galaxy’s history that are anom- 530, 783–799 (2000).
adapted for ice navigation, and capable of
alously enriched in radioactive thorium, and 7. Cowan, J. J. et al. Astrophys. J. 521, 194–205 (1999). accommodating sixty persons, will leave
at least one with uranium. We may expect 8. Goriely, S. & Clerbaux, B. Astron. Astrophys. 346, 798–804 (1999). Boston on or about June 26… The main object
of the voyage will be to offer to the members
of the excursion party opportunity of studying
Evolution the volcanic cones and lava-fields, the
geysers, ice-caves and glaciers of Iceland,
Infectious speciation the fiords and glaciers of the west coast of
Greenland, and the mountains and fiords of
Michael J. Wade Northern Labrador… A hunting party may
take part in the expedition; it could be landed
The bacterium Wolbachia has strange and wonderful effects on for a fortnight or three weeks in Greenland
reproduction in its many invertebrate host species. In effect, the creation and for about the same period in Labrador.
of new species can now be added to the list. From Nature 7 February 1901.

F
or a new species to arise, a single popu- 50 YEARS AGO
lation must somehow be split into two Males Females Surprisingly little of the information obtained
reproductively isolated populations with microscopes has been quantitative; most
that cannot interbreed. Such reproductive observers are content to sit at the microscope
No
isolation usually stems from genetic incom- and regard the image, or to photograph it.
X offspring
patibility. It is easy to see how that arises W+ Theoretically, it is possible to scan the image
W-
when a geographical barrier divides one or its photograph mechanically; but this has
population of an organism into two, which seldom been done in practice. The whole
then diverge genetically. On page 707 of this method of obtaining resolution by lenses
issue, however, Bordenstein, O’Hara and Offspring involves so much loss of light, lack of control
X
Werren1 show that in two species of para- W- W+ of contrast, and other difficulties, that it is
sitoid wasp it is microbial infection that is the difficult to provide a good display or method
barrier to gene exchange. of scanning. Some of these difficulties can be
The microbe concerned, Wolbachia pipi- Offspring avoided by using a wholly different means of
entis, is a member of a highly diverse group of X obtaining resolution and amplification. The
bacteria that is thought to include the ances- W+ W+ essence of the problem of resolution is to
tor of the mitochondrion — the powerhouse separate in some way the light passing
of multicellular organisms that was originally through very close regions of an object. The
free-living. Wolbachia are endosymbionts, Offspring conventional microscope does this by using
X
living inside the cells of certain host organ- W- W-
refraction by lenses to separate the light
isms, and like mitochondria they are almost from neighbouring regions. An alternative
always inherited through the maternal line. method is to use the lens system the other
Their host range is broad, for the bacteria are Figure 1 Wolbachia and cytoplasmic way round, namely, to produce a minute
found in association with about 20–75% of incompatibility. Cytoplasmic incompatibility spot of light. Discrimination between
the insects, crustaceans, mites and nematode means that when a male host infected with neighbouring points is then produced by
worms that have been surveyed with molec- Wolbachia (W& ) mates with an uninfected passing the light through them at different
ular markers2,3. Such is the range of effects female (W1 ), no offspring are produced. All times by making the spot scan it. After
of the microbe on its host — positive and other matings are fully compatible and result in passing through the preparation, the spot is
negative — that it is not always possible to the production of offspring. The consequence made to fall on a photocell, with subsequent
characterize Wolbachia simply as a mutual- of this system is that the maternally transmitted amplifcation and display as required. Such a
ist, symbiont or pathogen. Wolbachia tend to spread through the host flying-spot microscope depends on scanning
Among the variety of reproductive species. different parts at different times, and will
anomalies caused by Wolbachia is the only give accurate information about objects
phenomenon of cytoplasmic incompati- residing in host males are not typically that are stationary or moving only at a rate of
bility (Fig. 1), which results in the failure transmitted to offspring, but they eliminate a different order from that of the spot.
of infected host males and uninfected host competing uninfected maternal lineages From Nature 10 February 1951.
females to produce offspring. Wolbachia from the host population by their incompat-
NATURE | VOL 409 | 8 FEBRUARY 2001 | www.nature.com © 2001 Macmillan Magazines Ltd 675

86
news and views
ible matings. So the bacteria in males are Figure 2 Genetic and infectious models of
a
essential to the spread of their maternally speciation. a, A standard genetic model in which
Ancestral A 0 A 0 B0 B0
transmitted relatives through the host population the initial state is an ancestral population of a
population. Geographically
species that is homozygous at both of two gene
Typical cytoplasmic incompatibility falls isolated loci, and so is A0A0B0B0. Following geographical
daughter A 0 A 0 B0 B0 A 0 A 0 B0 B0
short of speciation because the barrier to populations
isolation, each of two daughter populations is
reproduction between infected and unin- gradually modified as new alleles (A1 and B1)
fected populations works only in one direc- Different arise by mutation and then become fixed in the
mutations
tion, not reciprocally. Although females become fixed genome by random genetic drift and natural
A 1 A 1 B0 B0 A 0 A 0 B1 B1
of the uninfected host population cannot in the genomes selection. Because the A1B1 gene combination
interbreed with males of the infected host causes complete inviability or sterility in
Reproductive
population, the reciprocal cross is fully isolation and hybrids, the daughter populations are new,
Mating results
fertile. But there is evidence4,5 that different speciation because
in inviable or
descendant species. b, Infectious speciation,
of the incompatible
genetic strains of Wolbachia can cause gene combination A1B1 infertile hybrids which parallels the genetic model. The initial
reciprocal, two-way reproductive isolation state is an ancestral species, W1 , not infected
b
between host populations in some parasitoid Uninfected (W-)
with Wolbachia. Two daughter populations
A 0 A 0 B0 B0
wasps, mosquitoes and fruit flies6. This ancestral W-
arise which have become infected by different
observation has led some evolutionary biol- population strains of Wolbachia (A and B) after
ogists to speculate that Wolbachia might Geographically A 0 A 0 B0 B0 A 0 A 0 B0 B0
transmission from a parasite or parasitoid. The
be an agent of infectious speciation6,7. isolated
W- W- different strains then become fixed in each
daughter
Such speculation is controversial, for two populations genome by cytoplasmic incompatibility.
reasons. First, it is widely accepted that, Reciprocal cytoplasmic incompatibility between
Independent
when two host populations become repro- infection and WA males and WB females, and WB males and WA
A 0 A 0 B0 B0 A 0 A 0 B0 B0
ductively isolated, so do the populations of spread of
WA
females, prevents hybridization, so in effect the
Wolbachia WB
their respective endosymbionts. Hence, in a daughter populations are new species even
process called co-speciation, a host may Reproductive though they remain genetically identical to one
cause subsequent speciation of its endo- isolation due to another and to the ancestor.
Reciprocal
Wolbachia
symbionts, an explanation suggested for the infection incompatibility
genetic divergence of strains of Wolbachia8.
The hypothesis of infectious speciation
turns this view on its head. Second, so the
theory goes, speciation occurs when repro- and natural selection operate independently How common might infectious speci-
ductive isolation arises as the incidental on each daughter population. Eventually, ation be? It is not possible to draw a con-
by-product of the gradualistic, genetic one gene undergoes mutation to allele A1, clusion from this single example — which
divergence of two populations. Microbial and becomes fixed in one daughter popu- has of course to be contrasted with the many
speciation, in contrast, might be compara- lation, while a second mutation, to allele B1 examples of genetic speciation10. But there
tively rapid (as seen for instance in polyploid at the other gene, becomes fixed in the sec- are several reasons why it is unlikely to
or hybrid speciation in some plants9), and ond daughter population. The two daughter happen often. First, incomplete cytoplasmic
could occur without any genetic evolution populations become reproductively isolated incompatibility (where incompatible cross-
of the host. Polyploid speciation occurs because matings between them result in the es produce some progeny instead of none)
through a doubling, or more, of chromo- A1B1 deleterious gene combination. In this seems to be more common than complete
some number. classic model, genetic barriers to reproduc- cytoplasmic incompatibility. Reciprocal but
Bordenstein and colleagues1 provide evi- tion and genetic exchange, and so speci- incomplete incompatibility is not a barrier
dence that microbes have acted faster than ation, arise as a by-product of local, gradual to gene flow. Second, genetic models of
genes in producing reproductive isolation evolution. Wolbachia–host coevolution indicate that
between the wasps Nasonia giraulti and N. Microbially driven speciation could the favoured trajectory is from complete
longicornis; this can be taken as the first stage occur in much the same way, stemming from to incomplete cytoplasmic incompatibility.
of speciation. First, the authors showed that cytoplasmic incompatibility between two Finally, we know little of the initial stages of
each wasp harbours a genetically distinct different strains of Wolbachia infecting the Wolbachia infection in natural populations.
strain of Wolbachia that causes cytoplasmic same host species (Fig. 2b). Here, however, When artificially introduced into new hosts,
incompatibility with the other uninfected infectious transmission of incompatible Wolbachia can be difficult to transmit11.
host species. They then used antibiotics to Wolbachia strains, one in each daughter pop- So the experimental results are consistent
create an uninfected strain of each host ulation, replaces the incompatible gene with the scheme outlined in Fig. 2b, but may
species and demonstrated that in Wolbachia- combinations. Predatory mites and para- not reflect the actual historical sequence
free wasps there are no genetic barriers in sitoid wasps are the most likely candidates of events.
first- or second-generation hybrids to free for spreading Wolbachia between different Nevertheless, with the paper by Borden-
interbreeding between the two wasps. species of host. Previous cases of reciprocal stein et al., host speciation can now be
How might these findings fit into a stan- cytoplasmic incompatibility have been added to the list of modifications to repro-
dard genetic model of speciation, as shown between species pairs, which also exhibited duction caused by Wolbachia infection.
in Fig. 2a? In this model, incompatible gene evidence of genetic barriers to gene Given the ubiquity of Wolbachia, infectious
combinations (such as A1B1) cause sterility exchange. Whenever both are present, it is barriers to gene exchange may be much
or inviability of offspring, and so speciation. difficult to determine which — the incom- more common in the early stages of speci-
Events begin with an ancestral species, patible gene combinations or the microbes ation than we realize. ■
A0A0B0B0, that becomes split by geological — came first. The report by Bordenstein Michael J. Wade is in the Department of Biology,
events into two geographically isolated et al. provides evidence that, at least in this Indiana University, Bloomington, Indiana 47405,
daughter populations. The evolutionary case, microbially induced reproductive iso- USA.
forces of mutation, random genetic drift lation preceded genetic isolation. e-mail: mjwade@bio.indiana.edu

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 news and views
1. Bordenstein, S. R., O’Hara, F. P. & Werren, J. H. Nature 409, 6. Hurst, G. D. D. & Schilthuizen, M. Heredity 80, 2–8 (1998). typical values. The first studies from this
707–710 (2001). 7. Thompson, J. N. Biol. J. Linn. Soc. 32, 385–393 (1987). period are now published in a special issue of
2. Werren, J. H., Windsor, D. & Gao, L. Proc. R. Soc. Lond. B 262, 8. Futuyma, D. J. Evolutionary Biology 541 (Sinauer, Sunderland,
197–204 (1995). MA, 1998). Geophysical Research Letters1.
3. Jeyaprakash, A. & Hoy, M. A. Insect Mol. Biol. 9, 393–405 (2000). 9. Reiseberg, L. H. Annu. Rev. Ecol. Syst. 28, 359–389 (1997). When the density dropped, many aspects
4. Wade, M. J., Chang, N. W. & McNaughton, M. Heredity 75, 10. Wu, C. I. & Palopoli, M. F. Annu. Rev. Genet. 28, 283–308 of the magnetosphere’s behaviour were as
453–459 (1995). (1994).
5. Shoemaker, D. D., Katju, V. & Jaenike, J. Evolution 53, 11. Clancy D. J. & Hoffmann, A. A. Am. Nat. 149, 975–988
scientists had predicted, which was a satisfy-
1157–1164 (1999). (1997). ing triumph for current theories. But the
event also had some puzzling characteristics.
Some of these are apparent in the data pre-
Astronomy sented in these initial papers, although not
all are commented on. Others aspects are so
The day the solar wind nearly died intriguing that further study is required.
Earth’s magnetic field is confined to the
Mike Lockwood low-density, high-field magnetosphere by
the dynamic pressure of the solar wind on the
On 11 May 1999, the density of the solar wind dropped almost to zero. side of the Earth facing the Sun, and by ther-
Space scientists are now giving their first reports of this rare opportunity to mal pressure on the long tail that trails away
study the complex relationship between the Sun and Earth. from the Sun (Fig. 1). Both these pressures
depend on the concentration of the solar
wind, so the magnetosphere grew to excep-

T
he study of space is generally passive, as solar wind, which varies in concentration,
the input factors to an environment flux, speed, temperature and composition. tionally large dimensions (100 times its typi-
cannot be adjusted in a controlled man- All of these factors affect the magnetosphere cal volume) as the solar wind decayed.
ner to study one isolated mechanism, as they — the cavity formed by the Earth’s magnetic Another feature was the appearance of high-
can in a laboratory. Instead scientists have to field in the solar wind — and separating their ly energetic flows of electrons parallel to the
monitor all the inputs and try to disentangle various effects is difficult. This is why rare direction of the magnetic field in the vicinity
the various effects that are taking place events such as the one centred around 11 of Earth. These so-called ‘strahl’ electrons
simultaneously. For instance, the Sun emits a May 1999 are so valuable. In this period, the (red arrows in Fig. 1) are continuously emit-
continuous stream of ionized gas (contain- solar wind remained completely normal ted by the Sun but their flow is usually dis-
ing mostly protons and electrons) called the except that its density plummeted to 5% of rupted by the solar wind, making their fluxes

a Figure 1 Earth’s magnetosphere and the solar

wind. a and b show two possible ways in which
the interplanetary magnetic field (IMF) can
Strahl
interconnect with Earth’s magnetospheric field.
a, New open field lines (red lines) are produced
IMF field lines Open
from the Sun field lines at a reconnection site XS and solar wind energy is
(XLN) directly deposited in the inner magnetosphere
XS Closed and upper atmosphere, as well as being stored in
field lines the tail of the magnetosphere because open field
To Sun Tail lines accumulate there. b, Field lines that are
Magnetosphere
Solar already open are reconfigured by reconnection
wind at XLN, in this example in the Northern
Hemisphere. In this instance, solar-wind energy
Cusp Open is not added to the tail because no new open flux
field lines
is produced. Closed field lines are shown in blue;
Bow shock Field lines to outer unconnected IMF lines are yellow; strahl
heliosphere electrons are represented by red arrows. The
Magnetopause
magnetopause is the boundary between the
magnetosphere and the solar wind, and the bow
b shock is the edge where the supersonic solar
wind abruptly drops in velocity. The solar wind
behind the bow shock (dark blue) is denser than
the incoming solar wind (medium blue),
XLN whereas the magnetosphere (grey) is the least
(XS) Open field lines dense of the three regions. A study of Earth’s
magnetosphere during a period of exceptionally
Closed field line low solar-wind flux promises to explain the
complex interplay between these
To Sun Magnetosphere Tail
Solar two situations1.
wind

Overdraped
open field line

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 letters to nature
for the separation of the moa, which was consistent with the estimated emu/cassowary .................................................................
Wolbachia-induced incompatibility
split at 30±35 Myr. The analysis was a simple extension of a described method29 to allow
more than four taxa. The assumption of rate constancy among the ratites was tested using
a likelihood ratio test of the molecular clock model30. With a likelihood ratio of 12.68, rate
constancy can be rejected (P , 0.01). However, Fig. 2 suggests that the ostrich may have an
elevated rate of substitution, so the test was repeated with the ostrich allowed a different
precedes other hybrid
rate from those of other ratites. The resulting likelihood ratio of 0.449 (P = 0.92) shows
that this two-rate model is consistent with clock-like behaviour. The two-rate model has incompatibilities in Nasonia
little effect on the divergence estimates (Table 2), with ostrich dates becoming younger by
5% of the largest change. Seth R. Bordenstein, F. Patrick O'Hara & John H. Werren
Received 12 July; accepted 26 October 2000.
Department of Biology, The University of Rochester, Rochester, New York 14627,
1. Cracraft, J. Phylogeny and evolution of the ratite birds. Ibis 116, 494±521 (1974). USA
2. Sibley, C. G. & Ahlquist, J. E. Phylogeny and Classi®cation of Birds (Yale Univ. Press, London, 1990). ..............................................................................................................................................
3. Cooper, A. et al. Independent origins of the New Zealand moas and kiwis. Proc. Natl Acad. Sci. USA
89, 8741±8744 (1992). Wolbachia are cytoplasmically inherited bacteria that cause a
4. Cooper, A. & Penny, D. Mass survival of birds across the Cretaceous±Tertiary: Molecular evidence. number of reproductive alterations in insects, including cytoplas-
Science 275, 1109±1113 (1997). mic incompatibility1,2, an incompatibility between sperm and egg
5. Feduccia, A. The Origin and Evolution of Birds (Harvard Univ. Press, Cambridge, Massachusetts, 1997).
6. Van Tuinen, M., Sibley, C. & Hedges, S. B. Phylogeny and biogeography of ratite birds inferred from
that results in loss of sperm chromosomes following fertilization.
DNA sequences of the mitochondrial ribosomal genes. Mol. Biol. Evol. 15, 370±376 (1998). Wolbachia are estimated to infect 15±20% of all insect species3,
7. Olson, S. L. in Avian Biology Vol. VIII (eds Farner, D. S., King, J. R. & Parkes, K. C.) 79±238 (Academic, and also are common in arachnids, isopods and nematodes3,4.
Orlando, 1985). Therefore, Wolbachia-induced cytoplasmic incompatibility could
8. Lee, K., Feinstein, J. & Cracraft, J. in Avian Molecular Evolution and Molecular Systematics (ed. Mindell,
D.) 173±208 (Academic, New York, 1997).
be an important factor promoting rapid speciation in
9. Houde, P. Ostrich ancestors found in the Northern Hemisphere suggest new hypothesis of ratite invertebrates5, although this contention is controversial6,7. Here
origins. Nature 324, 563±565 (1986). we show that high levels of bidirectional cytoplasmic incompat-
10. Bledsoe, A. H. A phylogenetic analysis of postcranial skeletal characters of the ratite birds. Ann.
ibility between two closely related species of insects (the parasitic
Carnegie Mus. 57, 73±90 (1988).
11. Cooper, A. in Avian Molecular Evolution and Molecular Systematics (ed. Mindell, D.) 345±373
wasps Nasonia giraulti and Nasonia longicornis) preceded the
(Academic, New York, 1997). evolution of other postmating reproductive barriers. The pre-
12. Handt, O., Krings, M., Ward, R. H. & PaÈaÈbo, S. The retrieval of ancient human DNA sequences. Am. J. sence of Wolbachia severely reduces the frequency of hybrid
Hum. Genet. 59, 368±376 (1996).
13. Krings, M. et al. Neandertal DNA sequence and the origin of modern humans. Cell 90, 19±30 (1997).
offspring in interspecies crosses. However, antibiotic curing of
14. Cooper, A. in Ancient DNA (eds Herrmann, B. & Hummel, S.) 149±165 (Springer, New York, 1993). the insects results in production of hybrids. Furthermore, F1 and
15. Boles, W. E. Hindlimb proportions and locomotion of Emuarius gidju (Patterson & Rich, 1987) (Aves: F2 hybrids are completely viable and fertile, indicating the absence
Casuariidae). Memoirs of the Queensland Museum 41, 235±240 (1997). of F1 and F2 hybrid breakdown. Partial interspeci®c sexual isola-
16. Lawver, L. A., Royer, J-Y., Sandwell, D. T. & Scotese, C. R. in Geological Evolution of Antarctica (eds
Thomson, M. R. A., Crame, J. A. & Thomson, J. W.) 533±539 (Cambridge Univ. Press, Cambridge,
tion occurs, yet it is asymmetric and incomplete. Our results
1991). indicate that Wolbachia-induced reproductive isolation occurred
17. Cooper, R. A. & Millener, P. R. The New Zealand biota: Historical background and new research. in the early stages of speciation in this system, before the evolu-
Trends Ecol. Evol. 8, 429±433 (1993).
tion of other postmating isolating mechanisms (for example,
18. Fleming, C. A. The Geological History of New Zealand and its Life (Univ. Auckland Press, Auckland,
1979).
hybrid inviability and hybrid sterility).
19. Stevens, G. R. Lands in collision. N. Z. Dept Sci. Ind. Res. Inf. Serv. 161 (1985). Symbiotic microorganisms are widespread in nature and often
20. Storch, G. in The Africa±South America Connection (eds George, W. & Lavocat, R.) 76±86 (Clarendon, have intimate associations with their hosts, ranging from mutua-
Oxford, 1993).
21. Martin, P. G. & Dowd, J. M. Using sequences of rbcL to study phylogeny and biogeography of
listic to parasitic relationships. It has been suggested that these
Nothofagus species. Aust. Syst. Bot. 6, 441±447 (1993). associations may act as a source of evolutionary innovation for their
22. Herzer, R. et al. Reinga Basin and its margins. N. Z. J. Geol. Geophys. 40, 425±451 (1997). hosts, leading to differentiation between host populations and
23. Sauer, E. G. F. Ratite eggshells and phylogenetic questions. Bonn Zool. Beitr. 23, 3±48 (1972). ultimately to the evolution of new species8. Wolbachia are particu-
24. Krause, D. W., Prasad, G. V. R., von Koenigswald, W., Sahni, A. & Grine, F. E. Cosmopolitanism
among Gondwanan Late Cretaceous mammals. Nature 390, 504±507 (1997).
larly good candidates for symbiont-induced speciation, because
25. Sampson, S. D. et al. Predatory dinosaur remains from Madagascar: Implications for the Cretaceous these bacteria can modify compatibility between eggs and sperm of
biogeography of Gondwana. Science, 280, 1048±1051 (1998). hosts, and thus directly cause reproductive isolation without long-
26. Cooper, A. & Poinar, H. Ancient DNA: Do it right or not at all. Science 289, 1139 (2000).
term coevolution of the host and symbiont5. There is some empiri-
27. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) (Sinauer,
Sunderland, Massachusetts, 1999). cal evidence for a role of Wolbachia in speciation in mushroom-
28. Huelsenbeck, J. P., Hillis, D. M. & Jones R. in Molecular Zoology: Strategies and Protocols (eds Ferraris, feeding Drosophila9, the ¯our beetle Tribolium10, and parasitic
J. & Palumbi, S.) 19±45 (Wiley, New York, 1996). wasps11. However, the view that Wolbachia are involved in inverte-
29. Rambaut, A. & Bromham, L. Estimating divergence dates from molecular sequences. Mol. Biol. Evol.
15, 442±448 (1998).
brate speciation is still controversial5±7. Here we present evidence
30. Felsenstein, J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. that Wolbachia-induced reproductive isolation precedes the evolu-
17, 368±376 (1981). tion of other postmating isolating mechanisms in Nasonia. The
®nding supports the view that Wolbachia can play a role in
Supplementary information, including clone and primer sequences is
available on Nature's World-Wide Web site (http://www.nature.com), or on
reproductive isolation and speciation.
http://evolve.zoo.ox.ac.uk/data/Ratites/, or as paper copy from the London editorial of®ce Nasonia is a complex of three closely related species of haplodi-
of Nature. ploid parasitic wasps. Nasonia vitripennis is found worldwide, and is
a generalist that parasitizes a variety of ¯y species. Nasonia giraulti
Acknowledgements occurs in eastern North America and N. longicornis in western
We thank W. Boles, R. Cooper, R. Herzer, P. Houde, C. Mourer-ChauvireÂ, D. Penny and North America, where they parasitize the pupae of blow¯ies in
T. Worthy for valuable comments, and M. Sorenson for allowing us access to unpublished birds' nests12. Genetic and molecular evidence shows that N. giraulti
rhea and ostrich sequences. We are grateful to T. Worthy and the staff of the Museum of and N. longicornis are more closely related sister species. Estimates
New Zealand for the moa samples. Modern samples were kindly provided by A. C. Wilson
(deceased), M. Potter and M. Braun, and laboratory space by R. Thomas, J. Bertranpetit
place the divergence of these two species at around 0.250 Myr ago
and the Oxford University Museum. A.C. was supported by the NERC, the Leverhulme and their divergence from N. vitripennis at around 0.800 Myr13.
Fund, the New Zealand Marsden Fund and the Royal Society. C.L.F. was supported by the All three species are infected with Wolbachia, and individuals of
Comissionat per a Universitats i Recerca (Catalan Autonomous Government), and A.R. each species are typically infected with two different bacterial types,
was supported by the Wellcome Trust.
each belonging to the two major subgroups of arthropod Wolbachia
Correspondence and requests for materials should be addressed to A.C. (e-mail: (A and B)14. Furthermore, phylogenetic analysis (data not shown)
alan.cooper@zoo.ox.ac.uk). Software is available at http://evolve.zoo.ox.ac.uk/software. indicates that the A group bacteria of each species are not closely
89

NATURE | VOL 409 | 8 FEBRUARY 2001 | www.nature.com © 2001 Macmillan Magazines Ltd 707
letters to nature
related to each other, and therefore have been independently their own species or males of the other species (N. giraulti female ´
acquired by horizontal transmission. Thus, the Nasonia system N. giraulti male, 100.2 6 5.6 versus N. giraulti female ´ N. longicornis
appears to be prone to the acquisition of Wolbachia, and is a male, 99.0 6 4.0; and N. longicornis female ´ N. longicornis
promising system for studying the role of these bacteria in repro- male, 68.5 6 4.1 versus N. longicornis female ´ N. giraulti male,
ductive isolation. 78.5 6 4.8). As only females are hybrids in a haplodiploid insect, we
Previous studies have shown Wolbachia-induced bidirectional also compared the number of female offspring produced in intra-
incompatibility between two diverged species, N. vitripennis and and interspeci®c crosses (Fig. 1). There was no reduction in the
N. giraulti11. F1 hybrids are not formed unless Wolbachia are number of F1 hybrid females relative to intraspeci®c controls.
removed by antibiotic curing. However, several other isolating Finally, we compared the number of eggs laid during a 6-h
barriers exist between these species, including high levels of F2 oviposition period to the number of adult offspring emerging in
hybrid lethality, abnormal courtship behaviours in F2 hybrid hybrid crosses. No signi®cant differences were found (N. giraulti
males (behavioural sterility), and partial premating (sexual) isola- female ´ N. longicornis male, 22.5 6 6.4 eggs versus 20.7 6 7.1
tion (refs 15, 16, and F.P.O'H., A C. Chawla and J.H.W., manuscript adults; reciprocal cross, 25.0 6 9.2 eggs versus 24.3 6 3.2 adults).
in preparation). It is therefore unclear whether Wolbachia-induced Therefore, results clearly indicate that there is no signi®cant F1
cytoplasmic incompatibility (CI) evolved before the evolution of hybrid inviability. They also show that there is no reduction in
other isolating barriers or after the divergence of the species. If fertilization of eggs based on whether the sperm came from hetero-
Wolbachia play a causal role in speciation, cases where Wolbachia- speci®c or homospeci®c males, indicating no incompatibilities in
induced CI evolved before other mechanisms of reproductive the fertilization mechanism between these species.
isolation should exist. The level of F1 hybrid female fertility was measured by counting
Here we investigate the role of Wolbachia in reproductive incom- eggs laid by females during a time-limited oviposition period. F1
patibility in a younger species pair, using the more closely related hybrid females did not show reduced fertility relative to non-hybrid
species N. giraulti and N. longicornis. First, we screened ®eld- control females (Fig. 2). In fact, hybrid females with the N. long-
collected insects to determine the frequencies of infections in icornis cytoplasm laid signi®cantly more eggs than non-hybrid
natural populations of the three species. A polymerase chain N. longicornis females (Mann±Whitney U-test (U), P , 0.001).
reaction (PCR) method was employed using previously published Sterility and/or mortality of F2 progeny (hybrid breakdown) is
speci®c primers17. In all three species, 100% of the individuals from one of the earlier manifestations of genetic incompatibility between
various geographical areas were found to be infected (N. giraulti, recently evolved species20,21. This is believed to be due to the general
n = 29; N. longicornis, n = 31; N. vitripennis, n = 31). All samples recessivity of genes involved in hybrid inviability and infertility20±22.
were doubly infected with A and B, except for one N. longicornis The haploidy of males in Nasonia offers an advantage to the study of
strain with a single A infection. Sequence analysis of PCR-ampli®ed recessive incompatibility factors, as such factors will be readily
products of the wsp gene18 from a subset con®rms that the species expressed in haploid males15,22. We investigated inviability by
are infected with species-speci®c Wolbachia, and that the Wolbachia comparing the number of F2 eggs laid by F1 virgin females to the
from different intraspeci®c strains form monophyletic groups (data
not shown), with little sequence variation within a host species.
We undertook experiments to determine whether Wolbachia a
cause reproductive incompatibility between the `young' species 100
Number of hybrid (female) offspring

pair, N. giraulti and N. longicornis. Wild-type infected strains and 90

antibiotically cured strains derived from those infected strains were 80
crossed in all pairwise combinations. Results show that bidirectional 70
CI occurs between infected N. giraulti and N. longicornis (Fig. 1). 60
When Wolbachia are present, no F1 hybrid (female) offspring are
50
produced in the N. giraulti male ´ N. longicornis female cross and
40
29.7 6 2.6 (mean 6 s.e., and hereafter) hybrid offspring are
30
produced in the reciprocal N. longicornis male ´ N. giraulti female
cross. In contrast, crosses using antibiotically cured strains produce 20
63.9 6 4.1 hybrid offspring and 82.9 6 5.1 hybrid offspring, 10
respectively. Thus, presence of Wolbachia causes a 100% reduction 0
GxG GxL LxG LxL
in F1 hybrids in one direction and 62.8% reduction in the other
Cross (female x male)
direction. In N. giraulti and N. longicornis, CI results in both a b
paternal genome loss19 and offspring lethality (data not shown). 100
Number of hybrid (female) offspring

These results show that Wolbachia-induced CI is a signi®cant 90

component of reproductive incompatibility between N. giraulti 80
and N. longicornis. 70
To assess whether Wolbachia-induced incompatibility between 60
N. giraulti and N. longicornis is one of the ®rst incompatibilities to 50
evolve in the divergence of these species, we tested for several other 40
hybrid incompatibilities. Speci®cally, we investigated (1) interspe-
30
ci®c sperm±egg compatibility, (2) inviability and sterility among F1
20
hybrid females and (3) inviability and sterility of F2 hybrid males.
10
Both spermatogenic and behavioural sterility of F2 males was
0
examined. All the experiments described below were performed GxG GxL LxG LxL
with uninfected individuals to exclude the effects of Wolbachia on Cross (female x male)
compatibility and viability.
To investigate viability of F1 females, we compared the number Figure 1 Number of hybrid (female) offspring produced from intra- and interspeci®c
of progeny produced by females mated to intra- and interspeci®c crosses. Results are shown for infected individuals (a) and uninfected individuals (b). Data
males. Crosses with uninfected females show that they produce are the mean number 6 s.e. of F1 progeny. G and L denote N. giraulti and N. longicornis,
the same number of F1 progeny whether they mate with males of respectively.
90

708 © 2001 Macmillan Magazines Ltd NATURE | VOL 409 | 8 FEBRUARY 2001 | www.nature.com
 letters to nature
number of F2 males that survived to adulthood. (Virgin females N. longicornis, 95.8% (n = 24); N. giraulti, 96.0% (n = 25);
produce haploid male progeny from unfertilized eggs in this X2 = 0.97, 2 d.f., P = 0.62). However, males did differ in their ability
haplodiploid insect.) There are no signi®cant differences in mor- to copulate with N. longicornis females (hybrids, 52.9% (n = 68);
tality levels among the F2 hybrid males relative to the non-hybrid N. longicornis, 95.2% (n = 21); N. giraulti, 21.2% (n = 19);
controls (Fig. 2). Mortality was found among F2 males of hybrid X2 = 22.74, 2 d.f., P , 0.001). This difference cannot be attributed
females from the N. longicornis male ´ N. giraulti female cross to hybrid breakdown, because hybrid males with N. longicornis
(mean 6 s.d. = 19.3 6 0.4% (ref. 23) mortality; U, egg versus adult females copulate at signi®cantly higher rates than do N. giraulti
number, p = 0.002). However, a similar level of mortality was also males (X2 = 6.08, 1 d.f., P = 0.014).
observed among non-hybrid N. giraulti males (F2 males from the The above results are therefore best explained as mate discrimi-
N. giraulti male ´ N. giraulti female cross; 14.3 6 0.3% mortality, P nation of N. longicornis females against F2 hybrid males, rather than
= 0.009). No signi®cant differences were found between these to F2 hybrid `sickness'. In contrast, our ®ndings with F2 hybrid males
crosses in the number of F2 eggs (U, P = 0.595) or F2 surviving from the older species pair (N. giraulti and N. vitripennis) indicate
adults (U, P = 0.862). Therefore, there is not elevated mortality high levels of reproductive incompetence throughout the various
among hybrids. This ®nding is quite different from what is found in stages of courtship and mating. For example in the older species
the older species pair (N. giraulti ´ N. vitripennis), which has high cross, 27.6% of F2 hybrid males failed to locate and mount females,
levels (70±85%) of F2 hybrid male mortality15. Such recessive and of those that did mount females, 26.8% failed to perform the
genetic incompatibilities have apparently not yet evolved between ritualized courtship display. As a result, a total of 53.2% of F2 hybrid
N. giraulti and N. longicornis. males in the older species cross fail to successfully mount females
We assessed the fertility of F2 hybrid and non-hybrid males by and perform the courtship display (compared to only 13.8% who
dissecting testes and categorizing sperm motility into three groups: fail to do so in the younger species cross, not signi®cantly different
normal, reduced or absent. All males possessed some motile sperm. from controls). We conclude that the genetic incompatibilities
The percentage of males with normal quantities of motile sperm was responsible for these problems have not arisen since the more
94.7% (n = 19) and 95.0% (n = 20) for the two hybrid genotypes and recent divergence of N. giraulti and N. longicornis.
95.0% (n = 20) and 100% (n = 19) for non-hybrids. Additionally, we Finally, we investigated the level of premating isolation between
tested the ability of hybrid and non-hybrid sperm to fertilize both the two species in single pair-mating situations. During a 30-min
N. giraulti and N. longicornis eggs. Of 69 males that copulated, only mating period, N. giraulti females show no mate discrimination
one failed to produce female offspring, but this occurred in an towards N. longicornis males, mating at similar frequencies as they
intraspeci®c cross. Thus, hybrid sperm is completely functional. do to homospeci®c males (94.5% mating, n = 200 versus 95.6%,
This contrasts to many studies in Drosophila, which indicate a n = 159, P = 0.32). In contrast, N. longicornis females show
prevalence of hybrid male sterility loci24,25 and that spermiogenic partial mate discrimination towards N. giraulti males relative to
sterility evolves rapidly in the divergence between species20,21. homospeci®c males (46.9% mating, n = 113 versus 89.9%, n = 178,
F2 hybrid breakdown can also affect courtship behaviour, due to a P , 0.0001).
general `sickness' of hybrid males or to speci®c negative interactions The experiments presented here clearly indicate that the species
in genes involved in courtship behaviour26. We assessed the ability of pair N. giraulti and N. longicornis do not show signi®cant levels of F1
hybrid and non-hybrid males to (1) locate and mount females, (2) or F2 lethality, F1 or F2 reproductive sterility, or F2 `hybrid sickness'
perform the ritualized courtship display, and (3) copulate with as manifested by competence in courtship behaviour. In contrast,
females. The type of female did not in¯uence probabilities of high levels of Wolbachia-induced reproductive incompatibility are
initiating courtship and no differences were found among males present in this species pair. Therefore, we conclude that interspecies
in their ability to locate and mount females (hybrids, 93.7% bidirectional CI has preceded the evolution of these other isolating
(n = 187); N. longicornis, 97.8% (n = 46); N. giraulti, 95.7% (n = 46); mechanisms in this system. In addition to Wolbachia-induced
X2 = 1.42, 2 degrees of freedom (d.f.), P = 0.49). Among males who reproductive incompatibility, there is partial premating isolation
successfully mount females, there was a small and nearly signi®cant in one direction between these species. The strength of premating
difference in the proportion of males performing the courtship isolation, at least under the conditions tested here, is weaker than
display (hybrids, 94.2% (n = 172); N. longicornis, 100% (n = 45); the postmating reproductive incompatibilities caused by Wolbachia.
N. giraulti, 100% (n = 45); X2 = 5.44, 2 d.f., P = 0.07). Among those The role of Wolbachia in speciation is a matter of current
males who courted N. giraulti females, no differences were found in debate5±7 and so far, there is limited empirical support for it9±11.
the proportion of males copulating (hybrids, 91.5% (n = 94); We do not claim that Wolbachia are currently causing reproductive
isolation between N. giraulti and N. longicornis in nature. Other
factors, such as geographical isolation (allopatry) are likely to be
more important. However, our results do show that Wolbachia-
30
induced bidirectional CI has preceded the evolution of other
25 intrinsic, postmating reproductive isolation barriers in these
newly evolving species. The present work therefore provides further
Offspring number

20
support for the argument that the cytoplasmic bacterium Wolbachia
15 could promote host speciation. M

10
Methods
5

0 Crosses for assay of CI and copulation frequencies

G[G] LG[G] GL[L] L[L] Single pairs of male and female virgins were observed for 30 min in a 12 ´ 75-mm vial. We
F1 female genotype only collected data on incompatibility relationships from crosses with an observed
copulation. After 24 h, the male was discarded from the vial, and each mated female was
Figure 2 F2 egg and adult offspring number produced from F1 hybrid and non-hybrid hosted with two Sarcophaga bullata blow¯y pupal hosts for egg laying. F1 progeny were
females. Data are the mean number 6 s.e. of eggs (black bar) and surviving adults (white scored for sex ratio and family size upon death. RV2, RV2R, IV7 and IV7R2 are the N.
giraulti and N. longicornis infected and uninfected strains, respectively. Uninfected strains
bar). The term in brackets denotes the cytotype, while the term before the brackets were generated from the corresponding infected strains in 1996 through antibiotic
denotes nuclear genotype. For instance, LG[G] hybrid females are derived from the cross, treatment of 1% Rifadin (10% sugar water) for three successive generations. Infection
L male ´ G female. status of these strains was con®rmed by PCR before the experiments.
91

NATURE | VOL 409 | 8 FEBRUARY 2001 | www.nature.com © 2001 Macmillan Magazines Ltd 709
letters to nature
F2 hybrid viability 26. Noor, M. A. F. Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila
pseudoobscura and Drosophila persimilis. Evolution 51, 809±815 (1997).
F1 hybrid and non-hybrid virgin adult females (1±2-d old) were placed on four hosts for
roughly 48 h for host feeding and egg laying. Females were immediately transferred to one
host for a 6-h laying period, after which females were removed from the vial. We limited Acknowledgements
the ovipositioning period to prevent wasps from becoming resource-limited. Half of these We thank R. Billings, M. Vaughn and B. J. Velthuis for technical assistance, and J. Bartos, A.
replicates were immediately scored for the number of F2 eggs laid in 6 h and the remaining Betancourt, J. Jaenike, J. P. Masly, T. van Opijnen and D. Presgraves for critical reading of
half were scored later for the number of adults. the manuscript. This work was supported by the NSF (J.H.W.).

Correspondence and requests for materials should be addressed to S.R.B.

Dissections for sperm motility assay (e-mail: sbst@troi.cc.rochester.edu).
Testes and seminal vesicles were viewed under a microscope at ´400 magni®cation for the
presence of motile sperm. Tested males were dissected on the day they emerged in a drop of
phosphate-buffered saline. At least one testis and one seminal vesicle from each male were
viewed. Males were scored as fully fertile if motile sperm were observed in all testes and
seminal vesicles observed. Males were scored as partially fertile if a reduced number of
motile sperm were observed in any organs viewed. .................................................................
F2 hybrid male behavioural and spermiogenic fertility Evolutionary radiations
Single males, aged 18±48 h, were placed in clear 12 ´ 75-mm vials with ®ve virgin females,
no more than four days old. Behaviour of each male was observed for 15 min. After and convergences in
courtship observation, males were left in the vial with females for an additional 105 min
(2 h total) and then removed. Females were then given ®ve hosts for feeding and egg laying. the structural
On death of their F1 progeny, each vial was inspected for the presence of female offspring,
indicating successful fertilization of at least one female by the tester male. Behavioural
fertility data were not signi®cantly different for F2 hybrid males from the two reciprocal
organization of mammalian brains
crosses (F2 males from N. giraulti males ´ N. longicornis females and from N. giraulti
females ´ N. longicornis males), and therefore the data were pooled for statistical Willem de Winter & Charles E. Oxnard
analysis.
Department of Anatomy and Human Biology, The University of Western
Received 22 September; accepted 30 November 2000. Australia, Perth, Western Australia 6907, Australia
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Univ. Press, Oxford, 1998). concerted enlargement of the whole brain4. However, interactions
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arthropod reproduction. Annu. Rev. Microbiol. 53, 71±102 (1999).
than concerted evolution. Here we analyse a large number of
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Massachusetts, 1991). show that the relative proportions of different systems of func-
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between Drosophila recens and Drosophila subquinaria. Evolution 53, 1157±1164 (1999).
10. Wade, M. J., Chang, N. W. & McNaughton, M. Incipient speciation in the ¯our beetle Tribolium
different mammalian orders, demonstrating separate evolution-
confusum: partial reproductive isolation between populations. Heredity 75, 453±459 (1995). ary radiations in mammalian brain organization8. Within each
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reproductive isolation between two insect species. Nature 346, 558±560 (1990).
similar behavioural niches and have convergently evolved similar
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Pteromalidae) reared from birds' nests in North America. Annals Enton. Soc. Amer. 83, 352±370 brain proportions. We conclude that within orders, mosaic brain
(1990). organization is caused by selective adaptation, whereas between
13. Campbell, B. C., Steffen-Campbell, J. D. & Werren, J. H. Phylogeny of the Nasonia species complex orders it suggests an interplay between selection and constraints.
(Hymenoptera: Pteromalidae) inferred from an rDNA internal transcribed spacer (ITS2). Insect Mol.
Biol. 2, 255±237 (1993).
We use data from the same source9,10 as the previous studies4,5. In
14. Werren, J. H., Zhang, W. & Guo, L. R. Evolution and phylogeny of Wolbachia: reproductive parasites of ref. 4 a small subset of these data was analysed multivariately to
arthropods. Proc. R. Soc. Lond. B 251, 55±71 (1995). study species separations, but in a context where size outweighed
15. Breeuwer, J. A. J. & Werren, J. H. Hybrid breakdown between two haplodiploid species: the role of most other information; an even smaller subset of the same data was
nuclear and cytoplasmic genes. Evolution 49, 705±717 (1995).
16. Bordenstein, S. R. & Werren, J. H. Effects of A and B Wolbachia and host genotype on interspecies
used to study bivariate relationships between pairs of brain parts in
cytoplasmic incompatibility in Nasonia. Genetics 148, 1833±1844 (1998). ref. 5. Here we examine the complete set of specimen measurements
17. Perrot-Minnot, M. J., Guo, L. R. & Werren, J. H. Single and double infections with Wolbachia in the underlying these data by relating the various brain structures in
parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics 143, 961±972 (1996)
proportion to two reference structures. We explore the detailed
18. Zhou, W. G., Rousset, F. & O'Neill, S. Phylogeny and PCR-based classi®cation of Wolbachia strains
using wsp gene sequences. Proc. R. Soc. Lond. B 265, 509±515 (1998). structure of the resulting 19-dimensional data space in two
19. Reed, K. M. & Werren, J. H. Induction of paternal genome loss by the paternal-sex-ratio chromosome stages, and combine the strategies of the previous studies4,5 by
and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. looking for species relationships as well as associations between
Mol. Reprod. Dev. 40, 408±418 (1995).
20. Wu, C. I. & Palopoli, M. F. Genetics of postmating reproductive isolation in animals. Annu. Rev. Genet.
variables.
28, 283±308 (1994). The ®rst stage in this study explores species separations in the
21. Orr, H. A. Haldane's rule. Annu. Rev. Ecol. Syst. 28, 195±218 (1997). subspace spanned by the ®rst three principal components (85% of
22. Gadau, J., Page R. E. & Werren, J. H. Mapping of hybrid incompatibility loci in Nasonia. Genetics 153, the information). Figures 1 and 2 show that all orders are clearly
1731±1741 (1999).
23. Mood, A. M., Graybill, F. A. & Boes, D. C. Introduction to the Theory of Statistics (McGraw Hill,
differentiated; this shows that they differ uniquely in their internal
Singapore, 1974). brain proportions. The three large ordersÐprimates, insectivores
24. Palopoli, M. F. & Wu, C. I. Genetics of hybrid male sterility between Drosophila sibling speciesÐa and batsÐare especially different, being dispersed in nearly ortho-
complex web of epistasis is revealed in interspeci®c studies. Genetics 138, 329±341 (1994).
gonal directions (although not along the orthogonal principal
25. True, J. R., Weir, B. S. & Laurie, C. C. A genome-wide survey of hybrid incompatibility factors by the
introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. components of the analysis). The primate and insectivore disper-
Genetics 142, 819±837 (1996). sions are separate, but are linked together via some bats. The two
92

710 © 2001 Macmillan Magazines Ltd NATURE | VOL 409 | 8 FEBRUARY 2001 | www.nature.com
Fruit odor discrimination and sympatric host race
formation in Rhagoletis
Charles Linn, Jr.*, Jeffrey L. Feder†, Satoshi Nojima*, Hattie R. Dambroski†, Stewart H. Berlocher‡,
and Wendell Roelofs*§
*Department of Entomology, New York State Agricultural Experimental Station, Cornell University, Geneva, NY 14456; †Department of Biological Sciences,
University of Notre Dame, Notre Dame, IN 46556-0369; and ‡Department of Entomology, University of Illinois, 320 Morrill Hall, 505 South Goodwin
Avenue, Urbana, IL 61801

Contributed by Wendell Roelofs, August 7, 2003

Rhagoletis pomonella is a model for incipient sympatric speciation standing sympatric host race formation and speciation in Rhago-
(divergence without geographic isolation) by host-plant shifts. letis, and potentially several other insect specialists, therefore
Here, we show that historically derived apple- and ancestral requires elucidating the mechanistic basis for differential host
hawthorn-infesting host races of the fly use fruit odor as a key choice. Here we show that host fruit odor plays a key role in this
olfactory cue to help distinguish between their respective plants. process.
In flight-tunnel assays and field tests, apple and hawthorn flies Precisely how R. pomonella distinguishes among potential
preferentially oriented to, and were captured with, chemical hosts is not known. However, studies have discerned several cues
blends of their natal fruit volatiles. Because R. pomonella rendez- that apple flies use to recognize apple trees. The major long-
vous on or near the unabscised fruit of their hosts to mate, the range stimulus drawing flies to apple trees appears to be volatile
behavioral preference for apple vs. hawthorn fruit odor translates compounds emanating from ripening apple fruit (13). In the
directly into premating reproductive isolation between the fly field, apple flies oriented upwind toward a point source of butyl
races. We have therefore identified a key and recently evolved hexanoate, a key component of the identified apple volatile
(<150 years) mechanism responsible for host choice in R. blend (Table 1), at a distance of 12 m (14). At shorter distances
pomonella bearing directly on sympatric host race formation and of ⬍1 m, visual cues become important for finding fruit within
speciation. the tree canopy (13, 15). Other visual characteristics of trees
(e.g., color, shape, and size), although used by flies for distin-
guishing trees from other objects (16), are not host-specific (13).
S peciation in sexual organisms occurs as inherent barriers to
gene flow evolve between previously interbreeding popula-
tions. To elucidate the origins of species therefore requires
The literature on host recognition in the R. pomonella apple race
therefore suggests that differences in fruit volatiles may be
understanding how and why new traits arise that reproductively critical for host discrimination.
To determine whether apple and hawthorn flies use fruit odor
isolate taxa (1). Proponents of sympatric or ecological speciation
as an olfactory cue to help distinguish between their host plants,
posit that divergence is often initiated as a result of natural
we prepared synthetic blends of apple and hawthorn volatiles
selection differentially adapting populations to alternative hab-
that contained the biologically active chemical components of
itats (2, 3). Habitat-specific mating is an ecological adaptation
fruit odors (Table 1; refs. 17 and 18). We then used these blends
central to many models of divergence-with-gene-flow speciation
in flight-tunnel assays and field trials to test whether apple- and
(4, 5). When organisms mate in preferred environments, a
hawthorn-origin flies preferentially oriented to, or were cap-
system of positive assortative mating is established that helps
tured with, their natal fruit volatiles. We report results implying
generate disequilibrium between habitat preference and perfor- that the historically derived apple fly race has evolved an
mance genes. This disequilibrium lessens the ‘‘selection- increased preference for apple fruit volatiles and decreased
recombination antagonism’’ (5, 6), making it potentially possible response to hawthorn volatiles.
for divergence to occur without geographic isolation in the face
of gene flow (i.e., in sympatry). Materials and Methods
The Rhagoletis pomonella sibling species complex is a model Insects. Apple and hawthorn flies were collected as larvae from
for sympatric speciation by host-plant shifts (7). The recently infested fruit in Grant, MI, Fennville, MI, and Urbana, IL,
derived apple (Malus pumila)-infesting population of R. during the 1999–2003 field seasons, and reared to adulthood in
pomonella, which originated by a shift from hawthorn (Crataegus the laboratory by using standard protocols (19). Apple and
spp.) in the mid-1800s, represents an example of host race hawthorn populations at these three sites have been the subject
formation in action, the hypothesized initial stage of sympatric of previous ecological and genetic studies and have been shown
speciation (2, 7). Host-specific mating is a key feature of to differ significantly from one another in allozyme frequencies
Rhagoletis biology, as it is for many phytophagous insect spe- (20–24). Eclosing adults were kept in cages in an environmental
cialists (2). Because Rhagoletis flies mate exclusively on or near chamber at 23–24°C, 16 h light兾8 h dark photoperiod, 60–70%
the unabscised fruit of its host plants (8, 9), differences in host relative humidity, and fed an artificial diet containing water,
preference translate directly into mate choice and premating sugar, vitamins, casein hydrolysate, and a salt mixture (25).
reproductive isolation (10). Rhagoletis is a vagile insect; most Sexually mature, odor-naive adults between 10 and 21 days
flies visit multiple trees in their lifetimes searching for food, posteclosion were tested in the flight tunnel. Roughly equal
mates, and fruit oviposition sites (10, 11). The potential there- numbers of males and females were tested, and no behavioral
fore exists for substantial mixing between sympatric fly popu- difference between the sexes was apparent in the flight tunnel.
lations. Despite this potential, fly migration has been estimated
to be 4–6% per generation per year (Rhagoletis is univoltine) Fruit Volatile Blends. Synthetic apple and hawthorn fruit volatile
between apple and hawthorn trees based on a mark-recapture blends were tested in the study (Table 1). The biologically active
experiment conducted at a field site with interspersed host trees
(10, 11). Studies on related sibling species in the R. pomonella
group have implied that ‘‘host fidelity’’ can potentially cause §To whom correspondence should be addressed. E-mail: WLR1@cornell.edu.
complete premating isolation between fly taxa (12). Under- © 2003 by The National Academy of Sciences of the USA

11490 –11493 兩 PNAS 兩 September 30, 2003 兩 vol. 100 兩 no. 20 93 www.pnas.org兾cgi兾doi兾10.1073兾pnas.1635049100
Table 1. Volatile blends for apple and hawthorn fruit 3-methylbutan-1-ol with the other components added in the
Apple blend Hawthorn blend proportions shown in Table 1. Blends were prepared 60 min
before the tests, with fresh sources and spheres used for each test.
Butyl hexanoate (0.37) Butyl hexanoate (0.01) Three treatments were tested: (i) a blank red sphere with a
Pentyl hexanoate (0.05) 3-Methylbutan-1-ol (1.0) control solvent-treated rubber septum, (ii) the apple blend, and
Propyl hexanoate (0.04) Isoamyl acetate (0.4) (iii) the hawthorn blend.
Butyl butanoate (0.1) 4,8-Dimethyl-1,3(E),7-nonatriene (0.02)
Hexyl butanoate (0.44) Ethyl acetate (20.0)
Field Trials. Field trapping studies were conducted in mixed-
Dihydro-␤-ionone (0.02)
variety apple orchards and hawthorn copses from August 27 to
The numbers in parentheses are microgram amounts per microliter of the September 9, 2002, at the Experiment Station in Geneva, NY,
solution applied to the septum. and from July 25 to September 5, 2002, at the Trevor Nichols
Research Complex near Fennville, MI. Red sphere traps (7.5-cm
diameter) coated with ‘‘Tanglefoot’’ stickum were used in New
chemical components of apple and hawthorn fruit volatiles were York, whereas clear glass spheres (5.5-cm diameter) were used
first identified by using solid-phase microextraction, coupled gas at the Michigan site to remove any visual cue provided by the red
chromatography兾electroantennogram detection, mass spec-
sphere. (Fig. 2 shows the spheres used in the study.) Three-way
trometry, and a sustained-flight tunnel assay (17, 18). The
choice experiments were performed to assess the relative pref-
compositions of the blends were determined through reiterative
erences of the host races for fruit odors. For the three-way tests,
testing such that equivalent amounts of whole-fruit extracts and
rubber septa lures containing 2 mg of apple, hawthorn, or no
the synthetic mixes elicited similar levels of behavioral activity
blend were separately attached to the tops of three spheres
from natal fly races in the flight tunnel (17, 18).
triangulated 2 m apart in host trees. Three replicate tests were
Flight Tunnel. The response of flies to fruit volatiles was measured conducted at each site in a trial period, with a trial period lasting
in a 183-cm-long, 61 ⫻ 61-cm-square flight tunnel (see refs. 17 from 1 to 2 days. Traps were checked after each trial period, with
and 18 for details of tunnel and flight conditions). Solutions of captured flies counted and removed, lures replaced, and traps
the synthetic blends prepared in hexane were applied to acetone- rotated to new positions. Statistical analyses were performed by
washed, rubber septa (Thomas Scientific, Swedesboro, NJ). A using the total number of flies captured across the three
septum was attached to a 7.5-cm-diameter red plastic sphere replicates during trial periods. Paired field trials of only the apple
(Great Lakes IPM, Vestaburg, MI) hung at the upwind end of blend vs. blank controls on clear spheres were also performed at
the tunnel. Individual flies were transferred to a screen cage, the Fennville, MI, site to assess host race attraction to apple odor
which was then placed on a screen stand 1 m downwind of the in the absence of the visual cue provided by the red sphere. For
sphere, and their behaviors were recorded (see Fig. 1 legend for the paired experiments, the apple blend was released from
description of fly behaviors). Field experiments have shown that scintillation vials prepared by Great Lakes IPM. Release rate of
apple flies can orient upwind to a point source of butyl hexano- odor from these vials was estimated at 1 mg兾h at 25°C. Baited,
ate, a key volatile of the apple odor blend, at a distance of at least clear spheres were hung 1 m from blank clear spheres fitted with
12 m (14). Fruit volatiles are therefore not just short-range empty vials. Six pairs of replicate traps were monitored and
attractants. For all flight-tunnel tests, 200-␮g sources of a rotated every 5 days for the paired trials. The same design was
particular fruit blend were used. For the apple blend, the 200-␮g used to test the apple blend in flowering dogwood (Cornus
dosage refers to the complete five-component mix (Table 1). For florida) stands in Cassopolis, MI, and Granger, IN, from Sep-
the hawthorn blend, the 200-␮g dose reflects the amount of tember 16 to October 13, 2002.

EVOLUTION

Fig. 1. Percentages of tested apple- (open symbols) and hawthorn-origin flies (filled symbols) displaying the indicated or greater behavioral acceptance of apple
blend (A) and hawthorn (Haw) blend (B) in flight-tunnel assays. Behavioral responses in order of increasing blend acceptance are as follows: walk and groom
(fly remaining in release cage), take flight (flight from the release cage), upwind (oriented flight toward sphere), and reach sphere. The percentage of flies
displaying walk-and-groom behavior ⫽ 100% ⫺ % take flight. Populations tested were ‚, Urbana, IL; ƒ, Urbana, IL, hawthorn flies reared on apple for two
generations; E, Grant, MI; 䊐, Fennville, MI; and 〫, Geneva, NY, apple fly colony. P ⬍ 1 ⫻ 10⫺7 for every test of behavioral difference between races at a site,
as determined by Fisher’s exact test. Populations within a race did not differ significantly from each other in their responses to their natal fruit blend. However,
significant heterogeneity occurred among apple-fly populations in their responses to hawthorn blend (G test reaching sphere ⫽ 11.3, P ⫽ 0.158, 3 df) and among
hawthorn fly populations to apple blend (G test ⫽ 15.8, P ⫽ 0.0006, 2 df).

Linn et al. 94 PNAS 兩 September 30, 2003 兩 vol. 100 兩 no. 20 兩 11491
Fig. 2. Tanglefoot-coated spheres used for field trials. (A) Clear sphere with
septum used to release volatiles for three-way choice tests at Fennville, MI. (B)
Clear sphere with scintillation vial used to release volatiles for paired apple-
blend vs. blank tests. (C) Red sphere used in New York field trials and flight
tunnel. Background is a hawthorn tree with red fruits visible.

Results and Discussion

Flight Tunnel. In control flight-tunnel experiments, no fly of either
host race flew upwind toward a ‘‘blank’’ red sphere fitted with
an odorless septum. The sphere and septum used as a release
point for the blends in the tunnel therefore held no intrinsic
attractive value from the 1-m distance at which flies were
released.
Significant differences were observed, however, in the behav-
ioral responses of the host races to red spheres with apple vs.
hawthorn volatiles. Virtually every apple-origin fly tested took
flight when the septum attached to the sphere contained the
apple blend. A majority of these apple flies (⬎70%) displayed
upwind anemotactic flight, tracking the apple-odor plume in the
tunnel to reach the source sphere (Fig. 1 A). The finding of
anemotactic flight, not previously reported for Rhagoletis, is
important because it implies that these flies have the capacity to
locate an olfactory source from a considerable distance in the
field. Hawthorn-origin flies responded similarly when the sphere
contained the hawthorn blend (Fig. 1B). However, both fly races
displayed a significantly reduced response to their nonnatal
blend. Less than 25% of apple flies flew upwind and reached the
sphere when hawthorn volatiles were present (Fig. 1B), and
fewer hawthorn flies reached apple-blend spheres (Fig. 1 A). The
results were similar for three pairs of apple and hawthorn fly
populations tested from Grant, MI, Fennville, MI, and Urbana, Fig. 3. Total percentages of resident Rhagoletis flies captured across repli-
IL, and for a laboratory colony of Geneva, NY, apple flies cate trapping periods on baited spheres (red in New York, clear in Michigan
established from the wild in the 1970s (Fig. 1). Thus, the host and Indiana) in apple orchards, hawthorn copses, and dogwood-tree stands in
races showed a consistent pattern of preference for their natal vs. Geneva, NY, Fennville, MI (FMI), Cassopolis, MI (CMI), and Granger, IN. (A)
nonnatal blend across their geographic range of overlap. More- Results for three-way choice study of apple blend, hawthorn blend, and blank
spheres. P ⬍ 1 ⫻ 10⫺12 for all pairwise comparisons of difference in fly capture
over, Urbana, IL, hawthorn flies reared for two generations in
on sphere types between apple orchard and hawthorn tree copses, as deter-
the laboratory on apple displayed the same behavioral responses mined by G contingency tests. (B) Results for paired field study of apple blend
as hawthorn flies reared directly from field-collected hawthorns vs. blank, clear spheres in apple, hawthorn, and dogwood tree stands. P ⬍ 1 ⫻
(Fig. 1). This finding discounts an effect of the larval-host fruit 10⫺15 for all comparisons of difference in capture on sphere types between
environment on adult fly behavior. Genetic crosses between apple vs. hawthorn or dogwood stands, as determined by two-tailed Fisher’s
apple and hawthorn flies are expected to allow mapping of exact test. Sample n ⫽ total number of flies trapped on all spheres in a given
quantitative trait loci for host odor preference. tree stand.

Three-Way Choice Study. Field trials indicated that the preferences

displayed by the host races in the flight tunnel were relevant in spheres across 12 replicate block periods; ␹2r for the Michigan
nature. In three-way choice experiments conducted in unsprayed apple orchard was 6.0; P ⫽ 0.05, three replicate periods). The
apple orchards near Geneva, NY, and Fennville, MI, resident pattern was reversed at hawthorn tree stands in New York and
flies were captured significantly more often on sticky spheres Michigan ⬍1 km away from the apple orchards (Fig. 3A). Here,
(red in New York, clear in Michigan) baited with the apple-blend significantly more flies were trapped on the hawthorn blend than
than on hawthorn-blend or blank spheres (Figs. 2 and 3A; ␹2r the other spheres (␹2r New York hawthorn stand was 12.7, P ⬍
Friedman’s test for the New York apple orchard was 21.1; P ⬍ 0.001, 12 replicate periods; ␹2r for the Michigan hawthorn stand
0.0001 for significantly higher rank order capture on apple-blend was 6.0, P ⫽ 0.05, 3 replicate periods).

11492 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.1635049100 95 Linn et al.

Paired Field Trials. The flight-tunnel and three-way choice exper- volatiles from apple fruit, and decreased response to hawthorn
iments imply that the historically derived apple race has evolved volatiles, during the course of its ⬇150 years of existence.
an increased preference for apple volatiles. To further test this Because mate choice in R. pomonella is directly tied to host
hypothesis, we performed paired field trails of just the apple choice, the difference in host odor preference results in premat-
blend vs. blank clear spheres at the Fennville, MI, site (Fig. 2B), ing reproductive isolation between apple and hawthorn flies. We
and a study of R. pomonella’s sister species, the undescribed
have therefore identified a key host-related adaptation under-
flowering dogwood fly (26). In the Fennville apple orchard,
significantly more resident flies were captured on the apple lying host race formation and incipient sympatric speciation in R.
blend than blank spheres (Fig. 3B; Z ⫽ 2.93, P ⫽ 0.003, pomonella.
two-tailed Wilcoxon sign-rank test for greater capture on apple In conclusion, investigations of the apple maggot fly are
blend spheres across 11 replicate periods). In the hawthorn tree adding to a growing list of systems demonstrating a role for
copse, in contrast, significantly more flies were captured on ecological adaptation in incipient population divergence and
blank spheres than on apple-blend spheres (Fig. 3B; Z ⫽ 2.52, speciation (3, 27–29). What makes the R. pomonella story
P ⫽ 0.012, eight replicate periods). The results in flowering compelling is that the known history and geography of race
dogwood stands were similar to those for hawthorn trees (Fig. formation allows us to directly connect host adaptation (e.g.,
3B). At two stands of C. florida trees near Granger, IN, and fruit-odor preference) and reproductive isolation in real-time
Cassopolis, MI, a total of 58 resident flies were captured on
apple-blend vs. 175 on blank spheres (Z ⫽ 2.52, P ⫽ 0.012, eight ecological experiments in nature.
replicate periods in Indiana; Z ⫽ 2.02, P ⫽ 0.043, five replicate
periods in Michigan). The reduced capture of both the ancestral We thank K. Catropia, K. Filchak, R. Harrison, C. Musto, R. Oakleaf,
hawthorn race and immediate outgroup dogwood fly on apple- K. Pelz, K. Poole, H. Reissig, J. Roethele, C. Smith, L. Stelinski, U. Stolz,
blend vs. blank clear spheres supports the hypothesis that the B. Westrate, J. Wise, the Niles, MI, U.S. Department of Agriculture
increased preference of apple flies for apple odor is a derived facility, the Trevor Nichols Research Complex, and the New York State
characteristic of the population. The results also suggest that Agricultural Experimental Station at Geneva Fly Rearing Center. This
hawthorn and dogwood flies may avoid the odor of apples. work was supported by grants from the National Science Foundation
Integrated Research Challenges (to all authors) and the U.S. Depart-
Conclusion. Our results imply that the apple race of R. pomonella ment of Agriculture National Research Initiative (to J.L.F. and S.H.B.)
has evolved an increased preference for a specific blend of and by the state of Indiana 21st Century Fund (to J.L.F.).

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Linn et al. 96 PNAS 兩 September 30, 2003 兩 vol. 100 兩 no. 20 兩 11493
 SEMINARIO III: GENÉTICA DE LA ESPECIACIÓN 
Marcela Rodriguero & Abel Carcagno 
 

En  este  seminario  se  discutirán  dos  trabajos  que  tratan  acerca  de  la  genética  de  la 
especiación  y  de  la  diferentes  escuelas  relacionadas  con  los  mecanismos  subyacentes  al 
proceso especiogénico. 
Nota:  Se  recomienda  especialmente  la  lectura  crítica  del  trabajo  “Dualism  and  conflicts  in 
understanding  speciation”,  de  Menno  Schilthuizen  (Bioessays  22(12):  1134‐1141,  2000) 
disponible en http://www.ege.fcen.uba.ar/materias/evolucion/material.htm 
 
Genética del proceso especiogénico: dos escuelas teóricas 
 
  Escuela Aislacionista  Escuela Seleccionista 
Punto  de  partida  de  la  Interrupción del flujo  Adaptación a ambientes 
especiación  génico  diferentes 
Fuerzas evolutivas  Deriva genética y/o  Selección natural 
preponderantes durante el  selección natural 
progreso de la especiación 
Resultado último de la  Aislamiento reproductivo  Diferentes acervos génicos 
especiación  pre y/o postcigótico  adaptados 
Velocidad del proceso  Más rápido en focos  Más rápido en simpatría, 
especiogénico en relación a  periféricos aislados,  aunque puede darse en otra 
la escala geográfica  aunque puede darse en otra  configuración geográfica 
configuración geográfica 
 
 

Escuela Aislacionista 
• Schemske D.W. & Bradshaw H.D. (1999) Pollinator preference and the evolution of floral 
traits in mokeyflowers (Mimulus). PNAS 96: 11910‐11915. 
 

1‐ ¿Existen los genes de la especiación? 
2‐ ¿Cuántos genes requiere un proceso especiogénico? 
3‐ ¿Qué son los QTLs y qué relevancia tienen para el estudio de la especiación? 
4‐ ¿Cuál es  la hipótesis  de trabajo de Schemske & Bradshaw (1999) y qué antecedentes la 
sustentan? 
5‐  ¿Qué  aproximación  experimental  utilizaría  para  dilucidar  la  arquitectura  genética  del 
aislamiento reproductivo mediado por polinizadores? 
6‐ ¿Cómo se confeccionó la figura 2? Indique el tratamiento estadístico de los datos. 

97
7‐  ¿Qué  conclusión  puede  extraer  de  la  figura  2  respecto  de  las  preferencias  de  cada 
polinizador? 
8‐  Explique  cómo  se  obtuvieron  los  resultados  graficados  en  las  figuras  3  y  4.  Compárelos 
con los de la figura 2. ¿Dichos resultados se contradicen? 
9‐ A partir de estos datos, ¿cuál es la arquitectura genética del aislamiento reproductivo de 
estas especies? 
10‐  ¿Se  puede  establecer  inequívocamente  que  los  cuatro  caracteres  analizados  son  los 
responsables absolutos del aislamiento reproductivo? 
 
Escuela Seleccionista 
• Fontaneto D., Ermiou E.A., Boschetti C., Caprioli M., Melone G., Ricci C., Barraclough T.G. 
(2007)  Independently  evolving  species  in  asexual  bdelloid  rotifers.  PLoS  Biology  5(4): 
914‐ 921. 
 
11‐ Si existen los genes de la especiación... ¿cuáles serían en este caso? 
12‐ ¿Qué particularidad presenta la clase Bdelloidea? ¿Qué concepto de especie utilizaría? 
¿Qué modelo de especiación? 
13‐  ¿Cuáles  son  las  hipótesis  del  trabajo  de  Fontaneto  et  al.  (2007)?  ¿Cuáles  son  las 
predicciones de cada escenario? 
14‐  Este  taxón  presenta  una  particularidad  que  podría  oscurecer  el  análisis.  Menciónelo  y 
fundamente su respuesta. A partir de dicha conclusión, ¿qué carácter emerge como la mejor 
opción para contrastar las hipótesis de trabajo y cuál podría ser su valor adaptativo? ¿Siente 
que  la  utilización  de  dicha  característica  podría  llevar  a  circularidad  en  el  contraste  de  la 
hipótesis? 
15‐  Una  vez  seleccionado  el  carácter  morfológico  a  estudiar,  mencione  los  fundamentos 
teóricos y las herramientas metodológicas utilizadas para abordar la hipótesis de evolución 
independiente. 
16‐  ¿Cuántas  entidades  evolutivas  se  pueden  distinguir  en  Bdelloidea?  ¿Son  realmente 
independientes? ¿Existe congruencia entre las unidades evolutivas y las reconocidas por los 
taxónomos? ¿Cómo explicaría las discrepancias? 
17‐  Mencione  la  aproximación  metodológica  y  teórica  utilizada  para  el  contraste  de  la 
hipótesis  de  divergencia  adaptativa  (relacione  esto  con  lo  aprendido  en  la  unidad  de 
Neutralismo). 
18‐ A partir de los resultados obtenidos, ¿qué fuerza evolutiva operó en la acumulación de 
cambio evolutivo dentro de Bdelloidea? ¿Qué factores apoyan este resultado? 
19‐  ¿Qué  unidades  evidencian  la  acumulación  de  divergencia  adaptativa?  ¿Se  le  ocurre 
alguna manera de reconciliar estos resultados con los derivados del contraste de la hipótesis 
de evolución independiente? 
20‐  Una  vez  comprendidos  los  objetivos  y  resultados  del  trabajo,  ¿cuántos  conceptos  de 
especie diferentes podría aplicar a los rotíferos de la clase Bdelloidea? 

98
Preguntas unificadoras 
21‐  Comparando  ambos  trabajos...  ¿En  qué  caso  la  selección  natural  desarrolla  un  papel 
principal en el proceso especiogénico? ¿Qué papel juega entonces en el otro caso de estudio 
durante el proceso de especiación? 
22‐ ¿Por qué cree que la teoría de especiación por selección natural tuvo menos adeptos en 
el pasado y actualmente está resurgiendo? 
 
 
 
 

99
Pollinator preference and the evolution of floral traits
in monkeyflowers (Mimulus)
Douglas W. Schemske*† and H. D. Bradshaw, Jr.‡

*Department of Botany and ‡College of Forest Resources, University of Washington, Seattle, WA 98195

Edited by Barbara Anna Schaal, Washington University, St. Louis, MO, and approved August 11, 1999 (received for review June 10, 1999)

A paradigm of evolutionary biology is that adaptation and repro- ondary contact. Two species that show this pattern of secondary
ductive isolation are caused by a nearly infinite number of muta- contact are the predominantly bee-pollinated Mimulus lewisii
tions of individually small effect. Here, we test this hypothesis by and its hummingbird-pollinated congener Mimulus cardinalis. M.
investigating the genetic basis of pollinator discrimination in two lewisii has pink flowers, a wide corolla with inserted anthers and
closely related species of monkeyflowers that differ in their major stigma, a small volume of nectar, petals thrust forward to provide
pollinators. This system provides a unique opportunity to investi- a landing platform for bees, and two yellow ridges of brushy hairs
gate the genetic architecture of adaptation and speciation because presumed to be nectar guides (Fig. 1A). M. cardinalis has red
floral traits that confer pollinator specificity also contribute to flowers, a narrow tubular corolla, reflexed petals, a large nectar
premating reproductive isolation. We asked: (i) What floral traits reward, and exserted anthers and stigma to contact the forehead
cause pollinator discrimination among plant species? and (ii) What of hummingbirds (Fig. 1C). Neither species has an odor detect-
is the genetic basis of these traits? We examined these questions able by humans, and our observations suggest that pollinator
by using data obtained from a large-scale field experiment where visitation is influenced primarily by flower color, size, shape, and
genetic markers were employed to determine the genetic basis of nectar reward.
pollinator visitation. Observations of F2 hybrids produced by cross- Despite striking morphological differences, these two mon-
ing bee-pollinated Mimulus lewisii with hummingbird-pollinated keyflowers are very closely related. A phylogeny based on DNA
Mimulus cardinalis revealed that bees preferred large flowers low sequence from the internal transcribed spacer of nuclear ribo-
in anthocyanin and carotenoid pigments, whereas hummingbirds somal RNA places M. cardinalis and the Sierra Nevada form of
favored nectar-rich flowers high in anthocyanins. An allele that M. lewisii together and distinct from Rocky Mountain and
increases petal carotenoid concentration reduced bee visitation by Cascade Range populations of M. lewisii and other members of
80%, whereas an allele that increases nectar production doubled the section Erythranthe (A. Yen, R. G. Olmstead, H.D.B. and
hummingbird visitation. These results suggest that genes of large D.W.S., unpublished work). Crosses between these two species
effect on pollinator preference have contributed to floral evolution produce fertile hybrids (20). Their geographic distributions are
and premating reproductive isolation in these monkeyflowers. This largely nonoverlapping, with M. lewisii found principally from
work contributes to growing evidence that adaptation and repro- mid-to-high elevation, and M. cardinalis found from low-to-mid
ductive isolation may often involve major genes. elevation. The two species co-occur in a narrow altitudinal zone
at 1400 m in the Sierra Nevada.
reproductive isolation 兩 adaptation 兩 speciation 兩 natural In 1998, we conducted observations (⬎80 hr) in a sympatric
selection 兩 pollination area along the South Fork of the Tuolumne River, California,
and found that bees were the only visitors to M. lewisii (100% of
233 visits), and that hummingbirds were the primary visitors to
O ne of the principal goals of evolutionary biology is to
discover the genetic architecture of adaptation. Fisher’s
‘‘infinitesimal’’ model of evolution proposes that adaptation is
M. cardinalis (97% of 146 visits). Only once did we observe a
pollinator visit both Mimulus species in succession. These results
show that pollinator discrimination results in strong premating
due to the fixation of many genes with small individual effects,
reproductive isolation in the zone of sympatry.
and is based on the assumption that large-effect mutations move
Two experiments are required to elucidate the genetic archi-
a population farther from, rather than closer to, its phenotypic
tecture of reproductive isolation by pollinator-mediated selec-
optimum (1). This micromutationist view of ‘‘adaptive geome-
tion. First, the genetic basis of traits such as flower color, size,
try’’ (2) has had widespread support, but was challenged recently
shape, and nectar reward must be determined for plant species
by a theory suggesting that mutations of large effect can often be
with different pollinators. Second, the response of wild pollina-
beneficial during the early stages of adaptation as populations
tors to each floral trait must be evaluated in a geographic region
move toward their optimum phenotype (3). There have been too
where the plant species co-occur. We have completed the first
few empirical studies to resolve the debate, and it is therefore
experiment, using linkage mapping with molecular markers to
important to identify systems in which both the genetic basis and identify quantitative trait loci (QTL) that control complex floral
ecological significance of adaptive traits can be identified (4, 5). traits in M. lewisii and M. cardinalis. We found that most floral
Adaptations that reduce the frequency of mating among traits had at least one QTL of large effect (explaining ⬎25% of
neighboring populations are of special interest, as these may the F2 phenotypic variance), suggesting that pollinator-mediated
contribute to the origin of new species. Although evidence from selection in this system could involve ‘‘major’’ genes (21, 22).
Drosophila suggests that premating isolation may evolve quickly Here, we report results from the second experiment, identifying
(6), and can have a simple genetic basis (7, 8), there are few the ecological significance of floral traits and the effect of simple
comparable data from other organisms and no studies investi- genetic changes on pollinator visitation in nature.
gating the genetics of premating reproductive isolation in natural
populations (9, 10).
Pollinator-mediated selection on floral traits is widely re- This paper was submitted directly (Track II) to the PNAS office.
garded as a common mechanism of adaptation and speciation in Abbreviation: QTL, quantitative trait loci.
plants (11–19). The traditional view is that adaptation to the †To whom reprint requests should be addressed. E-mail: schem@u.washington.edu.
most abundant or efficient pollinators in geographically isolated The publication costs of this article were defrayed in part by page charge payment. This
populations results in floral divergence, and that pollinator article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C.
preference prevents intercrossing if populations come into sec- §1734 solely to indicate this fact.

11910ⴚ11915 兩 PNAS 兩 October 12, 1999 兩 vol. 96 兩 no. 21 100

 EVOLUTION

Fig. 1. M. lewisii (A), an F1 hybrid (B), M. cardinalis (C), and examples of variation in floral traits found in F2 hybrids (D–L).

Materials and Methods outcrossed F2 population. The F1 hybrids have pink flowers and
moderately reflexed petals, with nectar guides similar to those of
Seed of both parental species was collected in Yosemite National M. lewisii, but lacking hairs (Fig. 1B), whereas the F2 generation
Park. We crossed M. lewisii (Fig. 1 A) with M. cardinalis (Fig. 1C) displays a wide range of flower colors and morphologies (Fig. 1
to produce F1 hybrids, then mated unrelated F1s to produce an D–L).

Schemske and Bradshaw 101 PNAS 兩 October 12, 1999 兩 vol. 96 兩 no. 21 兩 11911
 We examined the visitation by bees and hummingbirds to the
parental species and hybrids in an experimental population. We A 0.2
grew parental, F1, and F2 individuals to flowering in the Uni- Proportion of visits by bees
versity of Washington greenhouses as part of our QTL studies *

Standardized regression coefficient

(22), and transported a subset of these plants to the study site
(Wawona Ranger Station, Yosemite National Park, elevation 0.1
1300 m) where the two species co-occur. We arranged plants
randomly in a 5 x 15 m plot, with 0.5-m spacing (n ⫽ 24 for each
of the parents and the F1, and n ⫽ 228 for the F2 generation). 0
We used fewer parentals and F1s than F2s to reduce the
likelihood that pollinators would develop a preference for F2s
that resembled the parental species. Our observation period
-0.1
(June 1996) preceded the flowering time of natural populations
of M. lewisii and M. cardinalis. This schedule prevented gene flow
from our study population and ensured that pollinators had not
yet encountered the study species in natural populations in 1996. -0.2
We conducted observations of bee and hummingbird visita- **
tion from dawn to dusk in separate 30-min periods, three to four ***
times a day (mean ⫽ 3.7 periods per day for each pollinator type) -0.3
on 7 days from June 18 to June 27, for a total of 26 hr. Three to
five observers watched the plot during each observation period, ****
using tape recorders to record flower visits by bees and hum- anthocyanins
carotenoidsnectar
projected area
mingbirds. We recorded the number of open flowers for each B 0.4
plant on each day of observation. To obtain a daily ‘‘rate’’ of

Standardized regression coefficient

Visitation rates
pollinator visitation (visits per flower per day), we divided the
daily total number of visits for each pollinator by flower number.
****
There were more bees than could be recorded during some ****
observation periods, but this is likely to result in only a slight 0.2
underestimate of the relative frequency of bee visitation, so we *
did not attempt to correct for the unobserved bee visits. Voucher
specimens of the most common bees were identified by E.
Sugden (Department of Zoology, University of Washington).
Four floral traits were chosen for analysis: (i) petal anthocy- 0
anin concentration (purple pigments), (ii) petal carotenoid
concentration (yellow pigments), (iii) nectar volume, and (iv)
projected area (a composite measure of the petal surface
exposed to pollinators). These traits are highly diverged in the
two parental species (21–23), and were expected to affect
-0.2
*
pollinator visitation rates because of their contribution to pol- bees
linator attraction and reward. We cannot exclude the possibility hummingbirds
that other, unmeasured traits may contribute to pollinator
visitation, and that these may be linked to the traits included in -0.4
****
our study, or have pleiotropic effects on those traits.
We used the mean of two randomly drawn flowers per plant
antho. carot. nectar proj. area
to estimate the phenotypic value of each trait. Petal anthocyanin Fig. 2. Contribution of floral traits to pollinator visitation, as determined by
concentration was estimated by punching 6-mm disks from the multiple regression analysis (antho., petal anthocyanin concentration; carot.,
lateral petals, extracting the anthocyanins with 0.5 ml of meth- petal carotenoid concentration; nectar, nectar volume per flower; proj. area,
anol/0.1% HCl, and determining the absorbance at 510 nm. Petal projected area of petals). Bars give the standardized regression coefficients; 多,
carotenoid concentration was estimated similarly, using meth- P ⬍ 0.05; **, P ⬍ 0.01; ***, P ⬍ 0.001; ****, P ⬍ 0.0001. n ⫽ 228 F2 plants for
ylene chloride for extraction and measuring absorbance at 450 all analyses. (A) Multiple regression of floral traits on the proportion of visits
by bees (F ⫽ 24.2, P ⬍ 0.0001, R2 ⫽ 0.31). (B) Multiple regression of floral traits
nm. To estimate projected area of the corolla, we recorded video
on the mean daily visitation rates by bees (F ⫽ 22.1, P ⬍ 0.0001, R2 ⫽ 0.28) and
images of flowers from the perspective of approaching pollina- hummingbirds (F ⫽ 13.7, P ⬍ 0.0001, R2 ⫽ 0.20).
tors, i.e., in a plane perpendicular to the long axis of the corolla
tube, and analyzed these with image analysis software (National
Institutes of Health IMAGE; http://rsb.info.nih.gov/nih-image).
the composition of the pollinator assemblage, whereas analyzing
Nectar volume was measured with a graduated pipette tip. For
daily visitation rates by bees and hummingbirds identifies the
practical reasons, all measurements were conducted while the
study plants were growing in the University of Washington mechanisms responsible for differences in pollinator composi-
greenhouse. We remeasured a subset of plants in the field plot, tion, i.e., increasing bee visitation vs. decreasing hummingbird
and found that the greenhouse and field values were positively visitation. We performed an angular transformation on the
correlated for all morphological traits (P ⬍ 0.01, n ⫽ 56) and for proportion of visits by bees and a square-root transformation on
nectar volume (P ⬍ 0.0001, n ⫽ 31). all floral traits. The transformed variables were then standard-
To examine the relationship between pollinator visitation and ized (mean ⫽ 0, SD ⫽ 1) to provide a direct comparison of the
floral traits in the F2 population, we treated the proportion of magnitudes of the regression coefficients for different analyses.
bee visits and the daily visitation rates of bees and hummingbirds
as dependent variables in separate multiple regressions, with the Results and Discussion
four floral traits as independent variables. Analyzing the pro- We observed a total of 12,567 pollinator visits in the experi-
portion of bee visits evaluates the effects of floral characters on mental population. The non-native honeybee Apis mellifera

11912 兩 www.pnas.org 102 Schemske and Bradshaw

Fig. 3. Effect of allelic differences at the yup locus on the visitation rate (visits
per flower per day) of hummingbirds (A) and bees (B). Heterozygous individ-
uals (LC) or those homozygous for the M. lewisii allele (LL) lack carotenoids in
their upper petals and are pink-flowered (n ⫽ 165), whereas individuals
homozygous for the M. cardinalis allele (CC) have petal carotenoids and vary
in color from light orange to red (n ⫽ 63). Bars denote the mean ⫹ 2 SE.
Significance levels were determined by Mann–Whitney U tests.

comprised ⬍5% of the total visits to F2s and was excluded from

EVOLUTION
our analyses. We combined all other bee species to form a single
category. The bumblebee Bombus vosnesenski was responsible
for ⬎95% of all bee visits, with the remaining visitation by Osmia
(Monilosmia) sp. and an unknown bumblebee. Bumblebees
generally visited flowers for nectar and made only passive
contact with the anthers, whereas Osmia (Monilosmia) sp.
actively collected pollen during its foraging bouts. Pollen-
collecting bumblebees were observed most often on plants with Fig. 4. Effect of marker genotype for the major nectar QTL (RAPD marker
red or orange flowers. Anna’s hummingbird (Calypte anna) was L04co; ref. 22) on nectar volume per flower (A), and the visitation rate (visits
the only species of hummingbird observed. Although we did not per flower per day) of hummingbirds (B) and bees (C). Genotypes are: LL,
individuals homozygous for the M. lewisii allele (n ⫽ 61); LC, heterozygotes
mark hummingbirds, chases between individuals with different (n ⫽ 130); CC, individuals homozygous for the M. cardinalis allele (n ⫽ 36). Bars
plumage were common, suggesting that several different hum- denote the mean ⫹ 2 SE, and bars with different letters identify means that are
mingbirds were visiting the experimental plants. significantly different (P ⬍ 0.01) based on Mann–Whitney U tests corrected for
M. lewisii was visited primarily by bees (82% of 78 visits), and multiple comparisons (31).
M. cardinalis was visited by hummingbirds (99.6% of 2,097
visits), establishing that pollinator behavior in our experimental cating a strong genetic component to visitation. The composition
plots is similar to that observed in natural populations. The of pollinators visiting the F2s (8648 visits) varied widely, from
composition of the visitors to F1 hybrids (59% bees; 1,744 visits) plants visited only by bees to those visited only by hummingbirds,
was exactly intermediate to that of the parental species, indi- with a mean of 38% bee visitation per plant.

Schemske and Bradshaw 103 PNAS 兩 October 12, 1999 兩 vol. 96 兩 no. 21 兩 11913
 Increased petal anthocyanins, petal carotenoids, and nectar for the three F2 genotypic classes at the major nectar QTL (22).
volume significantly reduced the proportion of bee visitation, Our previous genetic mapping study found that this QTL
whereas greater projected area increased the proportion of bee explains 41% of the difference in nectar volume between the
visitation (Fig. 2A). These results provide clear evidence that two parental species and has an additive mode of action, with
f lower color contributes to reproductive isolation in this the M. cardinalis allele causing an increase in nectar (22).
system, despite recent statements to the contrary (24, 25). Segregation of the parental alleles at this locus produced a
Petal anthocyanin concentration significantly affected both nearly 3-fold range in mean nectar volume per f lower in our
bee and hummingbird visitation rates, but with opposite F2 field population (Fig. 4A). The average nectar volume of the
effects, whereas each of the other f loral traits had a significant heterozygous genotypic class was intermediate to that of the
effect on one pollinator, but not on the other (Fig. 2B). Bee two homozygous classes (Fig. 4 A), and the visitation rate of
visitation rate was negatively associated with petal anthocya- hummingbirds closely matched this distribution of nectar
nin and carotenoid concentration and positively associated volume (Fig. 4B). Plants homozygous for the M. cardinalis
with projected area, whereas hummingbird visitation rate was allele had twice the rate of hummingbird visitation as M. lewisii
positively associated with both petal anthocyanin concentra- homozygotes, whereas heterozygotes had an intermediate
tion and nectar volume (Fig. 2B). value (Fig. 4B). These results demonstrate that despite the
We tested the hypothesis that adaptation to different polli- bewildering array of f loral variation in the F2 population (Fig.
nators may involve genes with large phenotypic effects by 1 D–L), hummingbirds have the remarkable ability to distin-
comparing visitation rates as a function of QTL marker genotype guish the phenotypic effects of allele substitutions at the major
for petal carotenoid concentration and nectar volume, the two nectar QTL. In contrast, there was no relationship between
traits with the greatest impact on bee and hummingbird visita- bee visitation rate and marker genotype at the nectar QTL
tion, respectively (Fig. 2B). A single Mendelian locus controls (Fig. 4C). The ability of hummingbirds to quickly find rich
the distribution of carotenoid pigments in the petals (20). F2 nectar sources, and to return to them often, has also been
plants homozygous for the recessive M. cardinalis allele at the yup documented in experiments on spatial learning (29, 32, 33) and
locus (yellow upper; ref. 20) have carotenoids distributed suggests that hummingbirds are capable of exerting strong
throughout the petals, and are orange- or red-flowered (Fig. 1 selection on the nectar rewards of f lowers.
D, E, K, and L), whereas F2s carrying the dominant M. lewisii Taken together, our results provide evidence of striking
allele are pink-flowered (Fig. 1 F–J). There was no effect of yup differences in the floral preferences of bees and hummingbirds,
genotype on hummingbird visitation rate (Fig. 3A), but bee and considerable opportunity for the adaptive divergence of
visitation was 80% lower in plants homozygous for the M. floral traits through pollinator-mediated selection. This stands in
cardinalis allele (Fig. 3B). This clearly shows that genetic contrast to recent suggestions that pollinators typically have
variation for petal carotenoid concentration affects bee visi- broad preferences, and are therefore unlikely to contribute to
tation and supports earlier findings that bees visiting Mimulus floral evolution or the reproductive isolation of sympatric taxa
species in the section Erythranthe strongly prefer pink over red (25, 34, 35). Floral traits associated with bumblebee and hum-
f lowers (26). mingbird pollination, such as petal carotenoid pigments and
Although hummingbirds have been shown to exert strong nectar volume, appear to be under relatively simple genetic
selection for red coloration (27), we found only a weak rela- control, with major QTLs responsible for pollinator discrimina-
tionship between hummingbird visitation and flower color. tion and reproductive isolation in nature. This work contributes
Hummingbirds had a slight, but significant preference for flow- to the growing body of evidence that adaptation may often
ers with high petal anthocyanin concentration (Fig. 2B), but involve genes of large effect (3, 5, 36–39). Further studies are
exhibited no preference for flowers high in petal carotenoids. needed to determine whether our results can be generalized to
That petal carotenoids significantly decrease bee visitation but other plant taxa where closely related species differ in their
have no effect on hummingbirds suggests that the high concen- major pollinators.
tration of these pigments in the flowers of M. cardinalis (22) may
function primarily to discourage bee visitation. The hypothesis We thank B. Best, J. Coyne, and two anonymous reviewers for
that the red coloration of many hummingbird flowers functions thoughtful comments on the manuscript; B. Best, D. Ewing, B. Frewen,
J. McKay, K. Otto, Y. Sam, and K. Ward for technical assistance; E.
primarily to reduce visitation by insects (28) is consistent with Sugden for identifying the bees; and J. van Wagtendonk, P. Moore, and
the finding that hummingbirds do not have an innate preference the staff of Yosemite National Park for permission to conduct our
for red (29, 30). research. This work was supported by the Royalty Research Fund of
To examine the effect of nectar reward on pollinator the University of Washington and National Science Foundation Grant
visitation, we compared hummingbird and bee visitation rates DEB 9616522.

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EVOLUTION

Schemske and Bradshaw 105 PNAS 兩 October 12, 1999 兩 vol. 96 兩 no. 21 兩 11915
 PLoS BIOLOGY

Independently Evolving Species

in Asexual Bdelloid Rotifers
Diego Fontaneto1[, Elisabeth A. Herniou2,3[, Chiara Boschetti4, Manuela Caprioli1, Giulio Melone1, Claudia Ricci1,
Timothy G. Barraclough2,3,5*
1 Dipartimento di Biologia, Università di Milano, Milan, Italy, 2 Division of Biology, Imperial College London, Ascot, United Kingdom, 3 Natural Environment Research Council
Centre for Population Biology, Imperial College London, Ascot, United Kingdom, 4 Institute of Biotechnology, University of Cambridge, Cambridge, United Kingdom,
5 Jodrell Laboratory, Royal Botanic Gardens, Kew, United Kingdom

Asexuals are an important test case for theories of why species exist. If asexual clades displayed the same pattern of
discrete variation as sexual clades, this would challenge the traditional view that sex is necessary for diversification
into species. However, critical evidence has been lacking: all putative examples have involved organisms with recent or
ongoing histories of recombination and have relied on visual interpretation of patterns of genetic and phenotypic
variation rather than on formal tests of alternative evolutionary scenarios. Here we show that a classic asexual clade,
the bdelloid rotifers, has diversified into distinct evolutionary species. Intensive sampling of the genus Rotaria reveals
the presence of well-separated genetic clusters indicative of independent evolution. Moreover, combined genetic and
morphological analyses reveal divergent selection in feeding morphology, indicative of niche divergence. Some of the
morphologically coherent groups experiencing divergent selection contain several genetic clusters, in common with
findings of cryptic species in sexual organisms. Our results show that the main causes of speciation in sexual
organisms, population isolation and divergent selection, have the same qualitative effects in an asexual clade. The
study also demonstrates how combined molecular and morphological analyses can shed new light on the evolutionary
nature of species.
Citation: Fontaneto D, Herniou EA, Boschetti C, Caprioli M, Melone G, et al. (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biol 5(4): e87. doi:10.1371/
journal.pbio.0050087

Although horizontal gene transfer can occur between

Introduction
distantly related bacteria, homologous recombination occurs
Species are fundamental units of biology, but there remains only at appreciable frequency between closely related strains
uncertainty on both the pattern and processes of species [20,21]. Therefore, clusters in these bacteria could arise from
existence. Are species real evolutionary entities or convenient similar processes to interbreeding and reproductive isolation
figments of taxonomists’ imagination [1–3]? If they exist, what in sexual eukaryotes [20]. Aside from issues of sexuality,
are the main processes causing organisms to diversify [1,4]? previous studies looking for distinct clusters have been
Despite considerable debate, surprisingly few studies have descriptive, relying on visual interpretation of plots of
formally tested the evolutionary status of species [1,5,6]. genetic or phenotypic variation rather than on formal tests
One central question concerning the nature of species has of predictions under null and alternative evolutionary
been whether asexual organisms diversify into species [1]. The scenarios [1].
traditional view is that species in sexual clades arise mainly Here, we demonstrate that a classic asexual clade, the
because interbreeding maintains cohesion within species, bdelloid rotifers, has diversified into independently evolving
whereas reproductive isolation causes divergence between and distinct entities arguably equivalent to species. Bdelloids
species [7]. If so, asexuals might not diversify into distinct are abundant animals in aquatic or occasionally wet
species, because there is no interbreeding to maintain terrestrial habitats and represent one of the best-supported
cohesive units above the level of the individual. However, if clades of ancient asexuals [22–24]. They reproduce solely via
other processes were more important for maintaining parthenogenetic eggs, and no males or traces of meiosis have
cohesion and causing divergence, for example, specialization ever been observed. Molecular evidence that bdelloid
into distinct niches, then asexuals should diversify in a
manner similar to sexuals, although the rate and magnitude
Academic Editor: Mohamed A. F. Noor, Duke University, United States of America
of divergence might differ [8–11].
Empirical evidence to test these ideas has been rare. Most Received September 11, 2006; Accepted January 26, 2007; Published March 20,
2007
asexual animal and plant lineages are of recent origin [9,12].
The diffuse patterns of variation typical of such taxa [13] Copyright: Ó 2007 Fontaneto e al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
could simply reflect their failure to survive long enough for use, distribution, and reproduction in any medium, provided the original author
speciation to occur or the effects of ongoing gene flow from and source are credited.
their sexual ancestors [9,12]. Distinct genetic and phenotypic Abbreviations: GTR, general transition rate; PC, principal component; SEM,
clusters have been demonstrated in bacteria [14–17] and scanning electron microscopy
discussed as possible evidence for clonal speciation [1]. * To whom correspondence should be addressed. E-mail: t.barraclough@imperial.
However, all the study clades engage in rare or even frequent ac.uk
recombination as well as clonal reproduction [14,18,19]. [ These authors contributed equally to this work.

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 Speciation in Asexual Rotifers

Author Summary branches from other such clusters (H1, Figure 2A; and [9]).
Coalescent models can be used to distinguish the two
The evolution of distinct species has often been considered a scenarios [30]. Failure to reject the null model would indicate
property solely of sexually reproducing organisms. In fact, however, a lack of evidence for the existence of independently evolving
there is little evidence as to whether asexual groups do or do not entities.
diversify into species. We show that a famous group of asexual Next, to investigate the role of adaptation to different
animals, the bdelloid rotifers, has diversified into distinct species niches in generating and maintaining diversity within the
broadly equivalent to those found in sexual groups. We surveyed
clade, we extend classic methods from population genetics to
diversity within a single clade, the genus Rotaria, from a range of
habitats worldwide, using DNA sequences and measurements of jaw test directly for adaptive divergence of ecomorphological
morphology from scanning electron microscopy. New statistical traits. If trait diversity evolves solely by neutral divergence in
methods for the combined analysis of morphology and DNA geographic isolation, we expect morphological variation
sequence data confirmed two fundamental properties of species, within and between entities to be proportional to levels of
namely, independent evolution and ecological divergence by neutral genetic variation (H0, Figure 2B, Materials and
natural selection. The two properties did not always coincide to Methods). If, instead, different entities experience divergent
define unambiguous species groups, but this finding is common in selection on their morphology, we expect greater morpho-
sexual groups as well. The results show that sex is not a necessary logical variation between clusters than within them, relative
condition for speciation. The methods offer the potential for to neutral expectations (H1, Figure 2B; and [31]). Past work
increasing our understanding of the nature of species boundaries
has often discussed sympatry of clusters as evidence for niche
across a wide range of organisms.
divergence [1], but, in theory, coexistence can occur without
niche differences [32]; hence, we introduce an alternative,
genomes contain only divergent copies of nuclear genes more direct approach.
present as two similar copies (alleles) in diploid sexual Our results demonstrate that bdelloids have diversified not
organisms rules out anything but extremely rare recombina- only into distinct genetic clusters, indicative of independent
tion [25–27]. Yet, bdelloids have survived for more than 100 evolution, but also into entities experiencing divergent
million y and comprise more than 380 morphologically selection on feeding morphology, indicative of niche diver-
recognizable species and 20 genera [28]. The diversity of the gence. In common with findings of cryptic species in sexual
strictly asexual bdelloids poses a challenge to the idea that sex organisms [33,34], the morphologically coherent groups
is essential for long-term survival and diversification [29]. experiencing divergent selection often include several genet-
However, taxonomy does not constitute strong evidence for ic clusters: this introduces difficulties in deciding which units
evolutionary species: the species could simply be arbitrary to call species, but this problem is shared with sexual
organisms [3,33]. In short, bdelloids have diversified into
labels summarizing morphological variation among a swarm
entities equivalent to sexual species in all respects except that
of clones [7]. We adopt a general evolutionary species
individuals do not interbreed. The results demonstrate the
concept, namely, that species are independently evolving
benefits of statistical analyses of combined molecular and
and distinct entities, and then break the species problem into
morphological data for exploring the evolutionary nature of
a series of testable hypotheses derived from population
species.
genetic predictions [3]. We use the word ‘‘entity’’ to refer to a
set of individuals comprising a unit of diversity according to a
given criterion or test: the question of whether to call those Results/Discussion
entities ‘‘species’’ will be returned to below. We collected all individuals of Rotaria encountered during
Focusing on the genus Rotaria (Figure 1), one of the best- 3 y searching rivers, standing water, dry mosses, and lichens,
characterized genera of bdelloids, we use combined molec- centered on Italy and the United Kingdom but also globally
ular and morphological analyses to distinguish alternative [35]. Individuals were identified to belong to nine taxonomic
scenarios for bdelloid diversification (Figure 2). First, the species (Tables S1 and S2). Most of the described species of
entire clade might represent a single species, that is, a swarm Rotaria missing from our sample are known from only one
of clones with no diversification into independently evolving record or are very rarely encountered (Protocol S1). Bayesian
subsets of individuals. Second, the clade may have diversified and maximum parsimony analyses of mitochondrial cyto-
into a series of independently evolving entities. By ‘‘inde- chrome oxidase I (cox1) and nuclear 28S ribosomal DNA
pendently evolving,’’ we mean that the evolutionary processes sequences provide strong support for the monophyly of
of selection and drift operate separately in different entities taxonomic species (Figures 3, S1, S2, and S3 and Text S1),
[8,9], such that genotypes can only spread within a single with the sole exception of R. rotatoria, which was already
entity. Possible causes of independence include geographical suspected to comprise a species complex based on disagree-
isolation or adaptation to different ecological niches [10,17]. ments among authors [36,37].
The expected outcome is cohesion within entities but genetic Morphometric analyses further support the distinctness of
and phenotypic divergence between them [9–11]. taxonomic species. Bdelloid morphology is hard to measure
We first test for the presence of independently evolving because of their shape-changing abilities; hence, we used
entities. Under the null scenario of no diversification, genetic geometric morphometrics [38] to measure the only suitable
relationships should conform to those expected for a sample trait, their hard jaws, called trophi [39] (Figures 1 and S4).
of individuals from a single asexual population (H0, Figure Trophi size and shape are not characters that have been used
2A). Under the alternative scenario that independently in the traditional taxonomy of the genus (Table S2). Trophi
evolving entities are present, we expect to observe distinct scale weakly with rough measures of body size of each species
clusters of closely related individuals separated by long (mean trophi size against log body length from [37]: r¼0.55, p¼

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 Speciation in Asexual Rotifers

Figure 2. Scheme Showing the Predicted Patterns of Genetic and

Morphological Variation Underlying Our Tests of Alternative Scenarios of
Diversification
(A) Hypothetical trees showing expected genetic relationships among a
sample of individuals under the null model that the sample is drawn
from a single asexual population (H0) and under the alternative model
that the clade has diversified into a set of independently evolving
entities (H1).
(B) Expected variation in two ecomorphological traits evolving either
neutrally (H0) or by adaptive divergence (H1) in a genus that has
diversified into six genetic clusters. Note that a mixed pattern is possible:
Some genetic clusters may have experienced divergent selection on
Figure 1. SEM Pictures of Some Species of the Genus Rotaria morphology, whereas others have not.
doi:10.1371/journal.pbio.0050087.g002
(A) R. neptunia, lateral view; (B) R. macrura, ventral view; (C) R. tardigrada,
dorsal view; (D) R. sordida, lateral view; and (E) trophi of R. tardigrada
with open circles showing the location of landmarks used for the shape sordida, and R. tardigrada (Table S3). The remaining species
analysis. Scale bars: 100 lm for animals, 10 lm for trophi. overlapped in shape but could be discriminated by size
doi:10.1371/journal.pbio.0050087.g001 (Figures 4 and S5). Related species on the DNA trees tend to
have similar morphology: for example, R. magnacalcarata, R.
0.2, Spearman’s rank test), and both the size and shape of socialis, and R. rotatoria FR.2.1 and IT.5 overlap in shape, but are
trophi likely reflect different types or sizes of particulate food more distant from R. rotatoria UK.2.2. Only two of the
consumed, although the details of how food is processed traditional species found to be monophyletic in the DNA tree
remain unclear [28]. Discriminant analysis of the first five displayed significant variation in size or shape among
principal components (PCs) describing trophi shape (cumu- populations: R. sordida and R. tardigrada. In both cases, the
lative explained variance, 97.1%; Materials and Methods) populations that differed were deeply divergent in the DNA
produced a correct classification with respect to traditional tree as well.
taxonomy of most specimens of R. macrura, R. neptunia, R. Congruence between molecules and morphology confirms

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 Speciation in Asexual Rotifers

Figure 3. Phylogenetic Relationships in the Genus Rotaria

The consensus of 80,000 sampled trees from Bayesian analysis of the combined cox1 and 28S rDNA data sets is shown, displaying all compatible
groupings and with average branch lengths proportional to numbers of substitutions per site under a separate GTR þ invgamma substitution model for
the cox1 and 28S partitions. Posterior probabilities above 0.5 and bootstrap support above 50% from a maximum parsimony bootstrap analysis are
shown above and below each branch, respectively. Support values for within-species relationships are not shown for very short branches but are shown
in Figures S1 through S3. Closed circles indicate clusters identified by the clustering analysis. Colors represent traditional species memberships.
Diamonds indicate taxonomic species and monophyletic groups of Rotaria. Names refer to the species, the country, the number of site within that
country for that species, and the number of individual from that site if several were isolated; for example, R.macr.IT.1.1 refers to the first individual from
site 1 in Italy for R. macrura. Pictures of trophi from one individual from each cluster are shown to scale: Representatives of all sampled populations are
shown in Figure S4. A full list of names and localities of samples is available in Table S1.
doi:10.1371/journal.pbio.0050087.g003

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 Speciation in Asexual Rotifers

are present in bdelloids but at a lower level than taxonomic

species, that is, cryptic taxa within the taxonomic species.
However, the nature of independent evolution remains
unclear. Clusters might simply represent geographically
isolated, or even partially geographically isolated, populations
evolving neutrally [32,44]. Alternatively, the clade might have
diversified into ecologically distinct species experiencing
divergent selection pressures. To resolve these alternatives,
we test directly for divergent selection between different
lineages, adapting classic methods from molecular population
genetics [31,45]. If rotifers have experienced divergent
selection on trophi morphology between species, for exam-
ple, adapting to changes in habitat or resource use, we expect
low variation within species and high variation between
species, relative to the same ratio for neutral changes.
To explore the level at which divergent selection acts on
morphology, we compared rates of morphological change
within clusters, between clusters within taxonomic species,
Figure 4. Plot of the Size and Shape (the First Two PCs, PC1 and PC2, and between taxonomic species, in each case relative to silent
from the Generalized Procrustes Analysis) of Trophi across Species substitution rates in cox1, assumed to reflect neutral changes
The directions of shape variation along each axis are shown for PC1 and (see Materials and Methods). The test is robust to sampling
PC2, respectively, using 32 and 34 magnification of the observed issues and differences in mutational mechanism between
variation for emphasis. PC1 represents a continuum from oval to rounder morphology and cox1 (see Materials and Methods). The results
trophi and from parallel to converging major teeth. PC2 represents a
trend in the distance of the major teeth from the attachment point reveal significant evidence for divergent selection on trophi
between the two halves of the trophi. size and PC2 (Figure 5; Table S5). However, divergent selection
doi:10.1371/journal.pbio.0050087.g004 occurs between taxonomic species, not between clusters; both
traits are conserved within taxonomic species but diverge
that most traditional Rotaria species are monophyletic clades rapidly between species, relative to neutral expectations.
but does not rule out the possibility that taxa reflect variation Changes in PC1 are more complex, being lower between
within a single asexual species or swarm of evolutionarily clusters either than within clusters or between taxonomic
interacting clones. Under the alternative scenario that species. However, overall the results demonstrate divergent
independently evolving entities are present, we expect to selection on the size and some aspects of shape of the trophi.
observe clusters of closely related individuals separated from Our results show that Rotaria has undergone adaptive
other such clusters by longer internal branches on a DNA tree diversification in feeding morphology, presumably associated
[9,30,40]. We therefore tested for significant clustering by with specialization to different habitats. The finding is
comparing two models describing the likelihood of the supported by observations of ecological differences among
branching pattern of the DNA trees: first, a null model that the traditional species. For example, R. socialis and R.
the entire sample derives from a single population following magnacalcarata live externally on the body of the water louse
a neutral coalescent [41], and, second, a model assuming a set Asellus aquaticus but partition their use of the host, with the
of independently evolving populations joined by branching former living around the leg bases and the latter on the
that reflects the timing of divergence events between them, anterior, ventral surface. Our analyses show that these
that is, cladogenesis [9,30,42]. The models allow departures traditional species, which are found living together on single
from strict assumptions of constant population size and rates louse individuals, are evolutionarily independent and distinct
of cladogenesis (see Materials and Methods). entities. Another traditional species, R. sordida, is found in
The results indicate significant clustering within Rotaria, as more terrestrial habitats than the other species, although it
expected if several independently evolving entities are sometimes co-occurs with R. tardigrada, which is generally
present and consistent with patterns of mtDNA diversity more aquatic (Table S2). Therefore, informal observations of
from a broad sample of bdelloids [43]. The maximum habitat partitioning and coexistence at local scales add
likelihood solution for the independent evolution model on further support to the role of niche partitioning.
the combined tree infers 13 isolated clusters, with the Not all of the entities identified as genetic clusters display
remaining individuals inferred to be singletons (Figure 3; evidence of divergent selection on feeding morphology: the
Table S4). Two monophyletic taxonomic species contained signature of divergent selection was detected at a broader
two separate clusters: R. magnacalcarata has two clusters level than that of independently evolving clusters. One
corresponding to the U.K. and Italian samples, whereas R. possible explanation is that some clusters arose solely from
macrura has two clusters not matching sampling locality. neutral divergence in complete or partial geographical
Uncorrected pairwise distances of cox1 within clusters ranged isolation [32,44]. Some of the clusters do comprise geo-
from 0% to 3.3% (mean, 1.5%), and those between clusters graphically localized sets of samples, but at least one tradi-
ranged from 4.1% to 23.1% (mean, 16.0%). The null model tional species, R. macrura, contains two clusters without
that the entire lineage represents a single cluster can be obvious geographical separation. Alternatively, divergent
rejected (log likelihood ratio test, 2 3 ratio ¼ 30.8, v2 test, selection might act at different hierarchical levels on differ-
three degrees of freedom, p , 0.0001). ent traits [17]: clusters might have diverged in unmeasured
Our results indicate that independently evolving entities traits such as behavior, gross body morphology, or life history.

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 Speciation in Asexual Rotifers

model of reproductive isolation and neutral divergence

[32,47,48]? In addition, clades differing in levels of recombi-
nation could be compared to determine how sexual repro-
duction affects the strength and rate of diversification. Does
the requirement for reproductive isolation limit opportuni-
ties for speciation in sexuals, or do their faster adaptive rates
promote stronger patterns of diversification than in asexuals
[9,49]? Microbial eukaryotes, prokaryotes, and fungi could
provide additional study clades for such studies [12], linked to
genetic studies verifying the presumed lack of recombination
[50].
Our study highlights the advantages of statistical analyses
of combined morphological and molecular data. Recent work
delimiting or identifying species from DNA barcode data
[34,51] has been criticized for relying on organelle genome
markers, which may not reveal recent divergences or reflect
the history of nuclear genes [52,53]. Morphology provides a
ready window on adaptive differences between populations,
often the first sign of divergence and at the present easier to
sample than the genes underlying important traits [54,55], but
has lacked the theoretical framework of DNA. Combined
analyses, sampling at the population level across entire clades,
Figure 5. Evolutionary Rates of Changes in Trophi Size and Shape offer new potential to uncover the nature of species and
Rates are expressed as the variance in each trait per unit branch length. biological diversity. Our methods could be readily applied to
Branch lengths are in units of the number of silent substitution per
codon of cox1. Estimates from the maximum model with three rate
sexual clades and to other cases presenting challenges to
classes are shown: within clusters, between clusters within taxonomic current theories, such as groups in which barriers to
species, and between taxonomic species. Error bars show confidence interbreeding appear to be weak or nonexistent [1].
limits within 2 log likelihood units of the maximum likelihood solution.
Hierarchical likelihood ratio tests indicated that the model for size could
be simplified to assume a joint rate for within cluster and between Materials and Methods
cluster branches (Table S5).
doi:10.1371/journal.pbio.0050087.g005 DNA analyses. DNA was isolated either from clonal samples of five
to 25 individuals grown in the laboratory from a single wild-caught
individual or from single wild-caught individuals using a chelex
preparation (InstaGene Matrix; Bio-Rad, http://www.bio-rad.com).
Future work sampling additional genetic markers and The 28S rDNA and cox1 mtDNA were amplified and sequenced by
phenotypic traits for the identified clusters might distinguish PCR as described in Protocol S1. Trees were reconstructed from the
these alternatives. cox1 and 28S rDNA matrices separately and from a combined matrix
So which level should we call ‘‘species’’? As increasingly for all individuals with at least one gene sequenced. Bayesian analyses
were run in Mr Bayes (http://mrbayes.csit.fsu.edu) 3.1.1 for 5 million
recognized in reviews of species concepts, the answer will generations with two parallel searches, using a general transition rate
depend on which aspect of diversity is of most interest and on (GTR) þ invgamma model [56]. The combined analysis implemented a
the intended use of the delimitation [3,46]. For evolutionary partition model with a separate GTR þ invgamma model and rate
parameter for the two partitions. Maximum parsimony support was
studies, for example, into how bdelloids might adapt to assessed using 100 bootstrap replicates, searching each heuristically
changing environments, the genetic clusters provide statis- with 100 random addition replicates and TBR branch swapping in
tical evidence of independent evolution within the tradition- Paup*4.10. Eight individuals from the related genus Dissotrocha were
included as outgroups. Comparisons of the two genes are described in
ally recognized species that needs to be taken into account. Protocol S1 and Text S1.
For ecological studies, the traditional species conform closely Morphometric analyses. Trophi were prepared for scanning
to units that are ecologically distinct in terms of feeding electron microscopy (SEM) by dissolving soft tissues on a cover slide
morphology. Perhaps surprisingly for a poorly studied group with sodium hypochloride (NaOCl 4%), rinsing with deionized water,
dehydrating at room temperature, and sputter-coating a thin layer of
of microscopic animals, traditional species limits appear to gold. Shape was measured by Generalized Procrustes Analysis (GPA)
be robust for many purposes with the exception of the [57] of six landmarks on digitized pictures of the cephalic (ventral)
paraphyletic R. rotatoria. However, the important point here view (Figure 1). GPA coordinates were used for PC analysis after
projection onto an Euclidean space tangent to the shape space (see
is that the same issues apply to studies of sexual organisms. Protocol S1). Size was expressed as centroid size of the landmark
Genetic surveys often reveal cryptic species within morpho- configuration. We attempted to culture all individuals, to allow
logically coherent sexual species and elicit the same argu- morphometrics and sequencing on individuals from the same clone.
However, not all clones survived in the laboratory; for these, we used
ments over their interpretation [3,33,34]. replicate individuals from the same wild population where possible.
We conclude that bdelloids display the same qualitative In total, we measured 326 SEM pictures of trophi from 23
pattern of genetic and morphological clusters, indicative of populations belonging to eight species (see Table S1b). For species
with both laboratory-cultured and wild-caught measures, we found
diversification into independently evolving and distinct no evidence that sample type influenced either the mean or variance
entities, as found in sexual clades. This refutes the idea that of size and shape measures (Table S6), indicating respectively that
sex is necessary for diversification into evolutionary species. species differences are genetically based (not environmental) and that
Similar approaches could be used to explore the nature of there appears to be little genetic variation for morphology within
populations. Statistical analyses were performed using the R
species in sexual clades—for example, how often is speciation statistical programming language [58] and routines in the Tps series
accompanied by ecological divergence compared to a null of programs [59].

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 Speciation in Asexual Rotifers

Clustering test for independent evolution. Under the null model to each node. Below the branch are bootstrap percentages from a
that the entire sample derives from a single population obeying a maximum parsimony search with 100 bootstrap replicates each using
single coalescent process, we calculated the likelihood of waiting a heuristic search with 100 random addition replicates, TBR branch
times, xi, between successive branching events on the DNA tree as swapping, and saving only one tree per addition replicate.
x
Lðxi Þ ¼ b eb i
ð1Þ Found at doi:10.1371/journal.pbio.0050087.sg001 (21 KB PDF).

with Figure S2. Phylogenetic Relationships from Bayesian Analysis of cox1


b ¼ kðni ðni  1ÞÞ p
ð2Þ Posterior probabilities are indicated above each branch; parsimony
bootstrap values are indicated below each branch.
where ni is the number of lineages in waiting interval i, k is the Found at doi:10.1371/journal.pbio.0050087.sg002 (20 KB PDF).
branching rate for the coalescent (the inverse of twice the effective
population size in a neutral coalescent), and p is a scaling parameter Figure S3. Phylogenetic Relationships from Bayesian Analysis of 28S
that allows the apparent rate of branching to increase or decrease rDNA
through time, fitting a range of qualitative departures from the strict Posterior probabilities are indicated above each branch; parsimony
assumptions of a neutral coalescent, for example, growing (p , 1) bootstrap values are indicated below each branch.
or declining (p . 1) population size [30]. Under the alternative model
that the sample derives from a set of independently evolving Found at doi:10.1371/journal.pbio.0050087.sg003 (14 KB PDF).
populations, each one evolving similarly to the null case, we Figure S4. SEM Pictures of Trophi from Each Study Population
calculated the likelihood of waiting times as Equation 6 from Pons
et al. [30]. The alternative model optimizes a threshold age, T, such (A) R. macrura macrIT2; (B) R. macrura macrIT1; (C) R. macrura
that nodes before the threshold are considered to be diversification macrIT3; (D) R. macrura R.macr.UK.1; (E) R. magnacalcarata magnIT1;
events with branching rate kD and scaling parameter pD. Branches (F) R. magnacalcarata magnIT3; (G) R. magnacalcarata magnIT2; (H) R.
crossing the threshold define k clusters each obeying a separate magnacalcarata R.magn.UK.2.1; (I) R. socialis sociIT1; (J) R. socialis
coalescent process but with branching rate, kC, and scaling sociIT2; (K) R. socialis sociIT3; (L) R. socialis R.soci.UK, (M) R. rotatoria
parameter, pC, assumed to be constant across clusters. The R.rota.IT.5; (N) R. rotatoria R.rota.FR.2.1; (O) R. rotatoria R.rota.UK.2.2;
alternative model thus has three additional parameters. Models were (P) R. sordida sordIT1; (Q) R. sordida sordIT2; (R) R. sordida sordAU; (S)
fitted using an R script available from T.G.B. to an ultrametric tree R. neptunoida noidIT; (T) R. neptunia R.nept.IT, (U) R. tardigrada
obtained by rate smoothing the combined analysis DNA tree using tardIT1; (V) R. tardigrada tardIT3; (W) R. tardigrada R.tard.US; and (X)
penalized likelihood in r8s (http://ginger.ucdavis.edu/r8s) and cross- landmarks and links used for shape analysis.
validation to choose the optimal smoothing parameter for each tree Found at doi:10.1371/journal.pbio.0050087.sg004 (197 KB PDF).
[60].
Test for divergent selection. In an asexual clade, all genes have the Figure S5. Box Plot of the Size of Trophi for Each Study Population
same underlying genealogy: the entire genome is inherited as a single Analysis of variance test, ln CS: F22,303 ¼ 684.17, p , 0.0001.
unit. Assuming that silent substitutions are neutral, the expected
Found at doi:10.1371/journal.pbio.0050087.sg005 (56 KB PDF).
number of silent mtDNA substitutions on a branch of the genealogy
is lt, where t is the branch length in units of time and l is the Protocol S1. Sampling, Molecular Analyses, and Morphometrics
mutation rate of the gene. Assuming a neutral morphological trait
evolving by Brownian motion, the expected squared change Found at doi:10.1371/journal.pbio.0050087.sd001 (87 KB PDF).
(variance) along a branch is r2m t, where r2m is the mutational rate of Protocol S2. Test for Divergent Selection on Morphology
increase of variance [61]. The expectations are the same for branches
within populations or between them. Therefore, the average rate of Found at doi:10.1371/journal.pbio.0050087.sd002 (72 KB PDF).
change of a neutral trait expressed as variance per silent substitution Table S1. Locality Records for DNA Sequences and Morphometric
should be the same within populations as between them, that is, Measurements

r2m =l : This prediction holds even if mutation rates vary across the
tree, providing they do so without a systematic bias between the Found at doi:10.1371/journal.pbio.0050087.st001 (78 KB PDF).
branch classes being compared, a reasonable assumption shared with Table S2. Traditional Taxonomy of Rotaria Species
widely used molecular versions of the test [31].
We reconstructed evolutionary changes in trophi size and shape Found at doi:10.1371/journal.pbio.0050087.st002 (60 KB PDF).
(PC1 and PC2) onto the DNA tree using the Brownian motion model Table S3. Discriminant Analysis of Trophi Shape
by Schluter et al. [62] implemented in the Ape library for R [63].
Branch lengths were optimized as the proportion of silent sub- Found at doi:10.1371/journal.pbio.0050087.st003 (29 KB PDF).
stitutions per codon using PAML software [64]. The null model Table S4. Comparison of Models of Single versus Multiple Independ-
assumes a constant rate of morphological change across the entire ently Evolving Entities
tree. The alternative model labels branches as between taxonomic
species, within species and within clusters, and estimates different Found at doi:10.1371/journal.pbio.0050087.st004 (47 KB PDF).
rates for each class. Under a three rate-class model, the likelihood of Table S5. Comparison of Alternative Models for Rates of Changes in
the reconstruction, Equation 3 of [62] becomes the product of the Trophi Size and Shape within and between Clusters and Species
equivalent likelihood for each class of branches.
  Found at doi:10.1371/journal.pbio.0050087.st005 (37 KB PDF).
3 1 Qð~
lk Þ
Lð~l1:k ; b1:k Þ} P N1 exp ð3Þ Table S6. The Effects of Sampling Type (Clonal versus Population
k¼1 b
k
2bk
Sample) on the Mean and Variance of Size and Shape of Trophi
where k indicates the branch classes from 1 to 3, bk is the rate Found at doi:10.1371/journal.pbio.0050087.st006 (39 KB PDF).
parameter for each class of branches, Nk is the number of nodes
ancestral to each class of branch, and Q(ũk) is the sum of the scaled Text S1. Comparison of cox1 and 28S rDNA Results
variance of changes across branches [62] of class k. Optimization was Found at doi:10.1371/journal.pbio.0050087.sd003 (57 KB PDF).
implemented in a modified version of the ‘‘ace’’ function of Ape,
available from T. G. B. Divergent selection between taxonomic
species, for example, would be indicated by a significantly lower rate Accession Numbers
within cluster and within species branches (classes 1 and 2) than DNA sequences have been deposited at GenBank (http://www.ncbi.
between species branches (class 3). Assumptions and robustness of the nlm.nih.gov/Genbank) under accession numbers DQ656756 to
test are discussed further in Protocol S2. DQ656882.

Acknowledgments
Supporting Information
We thank Bill Birky, Jr., Austin Burt, Andrea Cardini, Fred Cohan,
Figure S1. Phylogenetic Relationships from Bayesian Analysis of the Brian O’Meara, Ian Owens, Andy Purvis, Vincent Savolainen, Michael
Combined Data Turelli, and two anonymous reviewers for their help.
Posterior probabilities from the Bayesian analysis are indicated next Author contributions. DF, EAH, GM, CR, and TGB conceived and

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 Speciation in Asexual Rotifers

designed the experiments. DF, EAH, CB, and MC performed the Association and The Linnean Society of London Systematics Fund
experiments. DF, EAH, CB, and TGB analyzed the data. GM, CR, and travel grant to DF, a Royal Society University Research Fellowship to
TGB contributed reagents/materials/analysis tools. DF, EAH, CR, and TGB, a Royal Society Dorothy Hodgkin Fellowship to EAH, and a
TGB wrote the paper. Royal Society International Joint Project grant to CR and TGB.
Funding. This research was supported by Natural Environment Competing interests. The authors have declared that no competing
Research Council UK grant NER/A/S/2001/01133, a Systematics interests exist.

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Problems and paradigms

Dualism and conflicts in

understanding speciation
Menno Schilthuizen

Summary first of these theories is the one put forward by Charles Darwin
Speciation is a central but elusive issue in evolutionary in 1859.(3) The second is the theory developed as part of the
biology. Over the past sixty years, the subject has been
studied within a framework conceived by Ernst Mayr and Modern Synthesis in the 1930s and 1940s. Since the theories
Theodosius Dobzhansky and subsequently developed differ chiefly in their emphasis on which factor drives popula-
further by numerous other workers. In this ``isolation'' tions apart, I will refer to them as the ``selection theory'' and the
theory, the evolution of reproductive isolation is a key ``isolation theory'', respectively.
element of speciation; natural selection is given only I will first recapitulate some aspects of the historical deve-
secondary importance while gene flow is considered
lopment of speciation theory, outline the basic tenets of both
prohibitive to the process. In this paper, I argue that
certain elements in this approach have produced confu- views, and highlight the conflicts between them. Then I will
sion and irreconcilability among students of speciation. review three prominent debates related to speciation and
The more prominent debates in speciation (i.e., the argue that all are reflections of those conflicts. At the same
species definition, sympatry/allopatry, and the role of time, I will describe recent data from field ecology, molecular
reinforcement) all derive from an inherent conflict
population genetics, laboratory experiments with Drosophila
between the ``isolation'' theory and Darwin's ``selection''
view on species and speciation (in which disruptive and computer analysis, which suggest that a modernised
selection is crucial). New data, mainly from field ecology, version of Darwin's view is more likely to bring progress in the
molecular population genetics, laboratory studies with field than an emphasis only on the isolation theory.
Drosophila and computer analysis, all suggest that the
isolation theory may no longer be the most desirable
vantage point from which to explore speciation. Instead, The conflict
environmental selection in large populations, often
Species and speciation form the basis of one of the longest-
unimpeded by ongoing gene flow, appears to be the
decisive element. The traditional preoccupation with standing debates in biology. Dedicated attempts to define
reproductive isolation has created gaps in our knowledge species were made as early as the 17th century.(4± 6) No single
of several crucial issues, mainly regarding the role of early author, however, devoted as much time to it as Darwin,
environmental selection and its connection with mate whose expertise in taxonomy made him the foremost authority
selection. BioEssays 22:1134±1141, 2000.
on species in the mid-19th century. In On the Origin of Species
ß 2000 John Wiley & Sons, Inc.
by Means of Natural Selection, he elaborated the point that
Introduction species are no more than ``well-marked varieties'', and that the
Speciation, the evolution of new species, is a central but un- term was ``arbitrarily given for the sake of convenience to a set
resolved issue in evolutionary biology.(1) What is the essence of individuals closely resembling each other''.(3) He added that
of speciation? What geographical conditions are required for it the ``search for the undiscovered and undiscoverable essence
to happen? What evolutionary forces are crucial? Many of the term species'' was in vain, as it was an attempt at
answers have been given to these questions and often appear ``defining the undefinable''.(7)
irreconcilable.(2) This has given rise to the conviction that Most present day biologists consider Darwin's opinion
speciation is a very multifarious phenomenon, which defies outdated and mainly accept the ``biological species concept''
any generalisation. As I will argue in this paper, this confusion (BSC). The BSC, which was developed during the 1930s by
stems largely from a conflict between two theories on specia- Ernst Mayr and Theodosius Dobzhansky, hinges (unlike
tion that have existed side-by-side for the past sixty years. The Darwin's concept) primarily on reproductive barriers. Mayr
defined species as ``groups of actually or potentially inter-
breeding natural populations, which are reproductively iso-
lated from other such groups''.(8) Dobzhansky consequently
applied the BSC to define the process by which species arise
Laboratory of Genetics, Wageningen University, Wageningen, The
Netherlands. Present address: Institute for Tropical Biology and
(i.e., speciation) as ``that stage of the evolutionary process at
Conservation, Universiti Malaysia Sabah, Locked Bag 2073, 88999 which the once actually or potentially interbreeding array of
Kota Kinabalu, Sabah, Malaysia. E-mail: schilthuizen@excite.com forms becomes segregated into two or more separate arrays
which are physiologically incapable of breeding''.(9)

1134 BioEssays 22.12 BioEssays 22:1134±1141, ß 2000 John Wiley & Sons, Inc.

114
 Problems and paradigms

It is important to realise that the BSC was not primarily able to make a single species change by adaptation, but also to
intended as a convenient criterion for sorting taxa. Instead, it make a single species split in two.
was an essential part of a multidisciplinary theory of specia- Darwin observed that an assemblage of species is more
tion. This theory developed in a number of logical steps. Mayr's efficient at exploiting a patch of habitat than a single species.
vast ornithological experience with geographic variation and By analogy, he reasoned that, under conditions of severe
endemism in New Guinea and Polynesia, and similar data from competition, natural selection will favour those individuals
other groups of organisms, had convinced him that geogra- within a population that have the most extreme phenotypes,
phical isolation (allopatry) was cardinal to the speciation and therefore suffer the least from competition with relatives.
process. His 1942 book Systematics and the Origin of ``Consequently, I cannot doubt that in the course of many
Species, was intended to show that the ``crucial process in thousands of generations, the most distinct varieties of any
speciation is not selection [ . . . ], but isolation''.(10) The fact that one species [ . . . ] would always have the best chance of
isolation was crucial meant that the processes responsible succeeding and of increasing in numbers, and thus of sup-
for allopatric differentiation would break down under gene planting the less distinct varieties; and varieties, when
flow. So, sympatry would only be possible once reproductive rendered very distinct from each other, take the rank of
isolation had evolved. In the absence of reproductive isolation, species''.(3)
two differentiated populations would fuse again upon second- The main difference between Darwin's view and the one
ary contact. Therefore, reproductive isolation needed to be elaborated by Mayr and Dobzhansky, then, is the role of
the decisive criterion for what constitutes a species, and the natural selection. To Darwin, natural selection could make a
evolution of reproductive isolation would define the point single population change to suit a changing environment
where speciation has been completed. (adaptation) or it could force a single population in two, to
The processes responsible for generating reproductive better exploit the available niches (speciation). Mayr and
isolation among populations were considered to be a subtle Dobzhansky, in contrast, decoupled adaptation from specia-
combination of genetic drift, natural selection, and epistasis, tion; environmental selection is a causative agent only in
acting in small ``peripherally isolated'' populations. Mayr adaptation. As I hope the following paragraphs will show, much
proved (1954, 1963) that, under the right circumstances, the of the confusion about speciation is the result of the fact that
combined effects of these forces could produce new co- the isolation theory has become embedded in the selection-
adapted gene complexes with reconstituted reproductive based neodarwinian school. Three conflicts in evolutionary
systems, i.e., new species under the BSC.(4,11) So, the theory biology are probably the direct result from this irreconcilability.
of speciation developed by Mayr and Dobzhansky relies These are the species definition, the allopatry/sympatry, and
almost exclusively on the evolution of reproductive isolation the reinforcement debates.
for explaining the origin and maintenance of species. To
many biologists, the development of this theory was an The species definition debate
improvement on Darwin, who had not realised the importance In Mayr's writings, two views on species appear. The first is
of reproductive isolation and hence lacked a clear theory on that all individuals of a species share the same well-integrated
speciation. complex of epistatically and pleiotropically interacting genes.
Both these claims about Darwin, however, are not entirely This is the species concept, and Mayr writes that the evolution
correct. Contrary to popular belief, Darwin was well-aware of of two well-integrated gene complexes from a single ancestral
reproductive isolation between species. For example, he one is ``the essence of speciation''.(4) At the same time,
starts chapter 8 of On the Origin of Species with: ``The view however, the biological species definition makes no mention
generally entertained by naturalists is that species, when of gene complexes, but rather of devices for reproductive
intercrossed, have been specially endowed with the quality of isolation. Consequently, Mayr can also be found writing that
sterility, in order to prevent the confusion of all organic ``speciation is characterized by the acquisition of these
forms''.(3) Darwin, however, knew that hybridisation is com- devices''.(4) What transpires is that Mayr did not claim that
mon among many groups of animals and plants, without reproductive isolation per se was essential, but that new
affecting the distinctness of species. This was one of the gene complexes can not evolve nor persist before such
reasons why he did not consider reproductive isolation of barriers to gene flow were in place: ``Reproductive isolation
crucial importance, writing that ``neither sterility nor fertility refers to the protective devices of a harmoniously coadapted
affords any clear distinction between species or varieties''.(3) gene pool against destruction by genotypes from other gene
To Darwin, then, speciation (or, as he called it, ``divergence of pools''.(4)
character'') was not brought about by the evolution of The contrast between Mayr's species concept (coadapted
reproductive barriers, but by a mechanism that would force a gene complexes) and his species definition (reproductive
single species in two directions, reproductively isolated or not. isolation) is illustrated by his discussion of cytoplasmic incom-
This mechanism was natural selection, which would not just be patibility in insects. This phenomenon, which is now known to

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Problems and paradigms

be caused by the bacterium Wolbachia,(12,13) can produce full occur without geographic isolation? If so, how easily, how
reproductive isolation between populations infected by differ- quickly and under what circumstances does it occur? In
ent strains of the symbiont. Hence, Laven(14) suggested that Darwin's theory of speciation (see above), sympatry is an
cytoplasmic incompatibility could be a mechanism for instan- implied prerequisite. Here, speciation is fueled by intraspecific
taneous speciation. Mayr,(4) however, objected that two competition. The most extreme phenotypes are selected,
cytoplasmically incompatible populations ``answer the defini- since they suffer least from mutual exclusion. By necessity,
tion of [...] species, yet there is serious doubt whether it would this process takes place only in full sympatry. In the isolation
be legitimate to label as species allopatric strains that may theory, on the contrary, there is no place for sympatry. Since in
differ by only a single genetic factor.'' Apparently, even though this framework any gene flow is expected to disrupt the
this single factor conveyed complete intersterility, Mayr hesi- evolution of new coadapted gene complexes, it is inconcei-
tated to apply the BSC, because the evolution of two different, vable that two different gene complexes could diverge within
coadapted gene complexes had not taken place.(15) the same population, without any prior reproductive isolation.
Recent molecular population genetic data, however, sug- Dobzhansky wrote: ``Species are distinct because they carry
gest that the BSC with its reproductive-isolation criterion does different constellations of genes. Interbreeding [ . . . ] results in
not automatically follow from a concept of a species as a co- a breakdown of these systems [ . . . ]. Hence, the maintenance
adapted gene complex, because the latter can persist in spite of species as discrete units is contingent on their isolation.
of the absence of reproductive barriers. In the fruit fly species Species formation without isolation is impossible''.(9)
complex Rhagoletis pomonella, for example, an estimated Empirical data exist for both allopatric and sympatric
gene flow of 6% does not negate the effects of disruptive speciation, however. On the one hand, Mayr's work remains
selection for an apple- and a hawthorn-feeding species.(16) one of the most comprehensive enumerations of evidence for
Another example comes from microsatellite studies of two allopatric speciation, listing numerous instances where popu-
European oak species. In spite of pervasive interspecific lations isolated by geographic barriers have genetically
hybridization and gene flow, the two sympatric species remain diverged to a small or large extent.(4) On the other hand,
morphologically, ecologically and genetically distinct.(17) evidence for speciation in sympatry has also been accumulat-
Furthermore, based on mtDNA and microsatellite data, ing steadily, especially in the past two decades. Some of this
vertebrate species(18,19) have been shown to exhibit consider- evidence is indirect: molecular phylogenetics of sympatric
able gene flow across ecotones. Nevertheless, this has not groups of freshwater fish in constricted environments (small
prevented the divergent environmental selection pressures lakes, the waters around rocky islands or a single stream
on either side of the ecotones resulting in the build-up of system) has revealed monophyly.(22± 24) Other evidence is
differently coadapted gene complexes.(20) more direct: observed host shifts in several groups of insects
These new data suggest that species differences can have led to the origin and maintenance of genetically differen-
persist in the face of gene flow. Therefore, the importance of tiated host-specialists.(25± 29)
``protective devices'' in the form of reproductive isolation These conflicting observations have produced a consen-
mechanisms may have been overstated. Consequently, since sus among many evolutionary biologists that speciation is
the relevant characteristics of species can also be attained multifarious. It can be allopatric, when it is caused by isolation,
without the protection of complete reproductive isolation, the or sympatric, when selection is the driving force. Differences of
case for using this property as a sine qua non for characterising opinion revolve primarily about the prevalence of either mode.
species has been considerably weakened. What remains is The two modes may not be so different, however, and, instead,
the valuable insight that species are stable coadapted gene they could be two ends of a continuum of gene-flow opport-
complexes. Disconnected from reproductive isolation, it is not unities, with selection as the driving factor across the range. To
possible or desirable to formalise this notion into a strict assess the merits of this view, it may be worthwhile to investi-
species definition. In evolutionary biology, it should be suf- gate in more detail the respective roles of selection and iso-
ficient to study the evolution of such gene complexes, without lation in allopatry.
any reference to the category assigned to them. In taxonomy, To begin with the latter, indications exist that even in
the BSC has only incidentally been used as a standard to test classical cases of allopatry (populations isolated in caves, on
systematic revisions against and Darwin's motto that ``the islands, or in habitat fragments) residual gene flow remains
opinion of naturalists having sound judgement and wide among the supposedly isolated populations. Populations of
experience seems the only guide to follow'',(3) has never cave organisms, for example, have been shown to be inter-
ceased to be important. connected by subterranean populations living in minute rock
crevices,(30) while land snail populations on isolated limestone
The sympatry/allopatry debate hills probably exchange genes via low-density populations on
The single most conspicuous conflict in speciation undoubt- non-calciferous soils.(31) The degree of isolation, then, may
edly is the sympatry/allopatry debate.(1,4,21) Can speciation often have been overestimated.

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The role of selection, in contrast, may have been under- gence corresponds well with the geological age of the barrier.
valued in models of allopatric speciation. In the basic allopatry Nevertheless, there can be no doubt that the populations have
model, a species' range becomes bisected by a physical always been very large, which rules out any bottleneck effects
barrier, producing two very large daughter populations. With or genetic drift. In contrast, transisthmian environmental
this model, since selective differences are likely to be small, differences are considerable, including tidal influence, nutrient
and the populations so large that genetic drift is close to zero, content and temperature fluctuations, which might better
speciation will proceed slowly, if at all. Stebbins,(32) for explain the genetic differentiation.
example, pointed out that American and Asian sycamore Laboratory studies, too, have shown that reproductive
trees, after millions of years of isolation, have failed to evolve isolation can build up in ``allopatric'' populations exposed to
reproductive isolation. According to Mayr,(33) the rise of the different selection regimes. Rice and Hostert(34) cite numerous
Isthmus of Panama, which partitioned entire marine biotas into experiments using Drosophila that resulted in prezygotic
a Pacific and a Caribbean portion 3.5 million years ago, had reproductive isolation. Some experimenters(43,44) also tested
produced ``two collossal gene pools'', and ``differences are still the development of reproductive isolation between allopatric
either nonexistent or they are so slight that one doesn't really populations that experienced the same selection pressure,
like to rank these as species.'' and obtained negative results. These developments indicate
In the isolation framework, where founder effects and that in both allopatric speciation and sympatric speciation,
genetic drift play an important role, large isolated populations adaptation to different niches is the driving force, although
are not expected to be the ideal situation for the evolution stronger selection pressures are required to produce specia-
of new coadapted gene complexes. Stebbins's sycamore tion in the latter. This selection pressure will often be met
enigma, for example, was explained by Mayr(4) by arguing that because of strong competition in sympatry.
the two populations had been too large to be genetically
restructured and hence continued to share the same balancing The reinforcement debate
systems. An alternative for basic allopatry is the bottleneck The reinforcement model of speciation says that populations
model, in which geographically isolated populations are that have attained a certain degree of postzygotic reproductive
founded by a very small number of colonists. In such a small isolation in allopatry (as shown by reduced hybrid fitness),
population, random changes in gene frequencies and the are expected to improve prezygotic reproductive isolation
ensuing changes in epistasis could, theoretically at least, on secondary contact, given natural selection for assortative
cause a genetic revolution, leading to a new coadapted gene mating.(9,45± 47) In view of its reliance on reproductive isolation
complex, which subsequently could possibly shift into a new alone, reinforcement can thus be seen as fully consistent with
niche. the ``isolation'' view of speciation.
Little evidence for bottleneck speciation exists, however. To better define the role of reinforcement in speciation,
Five small-scale(34) and three large-scale(35 ±37) laboratory Butlin distinguished between the processes of reproductive
studies have largely yielded negative results. Molecular data character displacement (namely, the adaptive increase of
from field populations also do not support the idea. Ancient assortative mating between populations that have already
allele polymorphisms in island species flocks, long regarded experienced full postzygotic reproductive isolation) and
as prime examples of speciation by founder effects, were dis- reinforcement (that is, adaptive increase of assortative mating
covered to be high. Enzyme polymorphisms in the Hawaiian between populations that have experienced only partial
Drosophilas are just as high as those in their mainland postzygotic reproductive isolation).(45,46) With this distinction
counterparts,(38) and in the GalaÂpagos finches, 21 ancient in mind, we see that reproductive character displacement is
allele variants were found at an Mhc locus.(39) The persistence not a speciation process under the isolation theory, whereas
of high numbers of ancient haplotypes is inconsistent with very reinforcement is. Nevertheless, the basic evolutionary me-
small numbers of colonists. In the case of the GalaÂpagos chanism (selection for assortative mating) is identical in both
finches, the founding populations must at least have been as processes.
large as forty birds, and probably several hundred. Butlin's papers, which also carried criticism against the
At the same time, new data tend to favour the basic probability of reinforcement actually operating in nature, were
allopatry model. The Panama Isthmus, regarded by Mayr as followed by a number of theoretical,(47 ±49) comparative(50,51)
ineffective in producing allopatric speciation, is now known and empirical(52,53) studies. Liou and Price(49) showed that,
to have caused the evolution of numerous reproductively under conditions of low hybrid fitness and considerable initial
isolated species in various groups of marine organisms.(40) genetic divergence between the two hybridising populations,
Knowlton and co-workers(41,42) for example, have shown that reinforcement could indeed reduce gene flow to zero. The
the isthmus separates almost twenty pairs of sister species of empirical studies, which were done on flycatchers(53) and
snapping shrimp. All species pairs are reproductively isolated Drosophila,(52) supported this, as they showed an increase in
while morphologically very similar, and their mtDNA diver- assortative mating in sympatry, whereas hybrid fitness was

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low but not zero. The comparative studies on Drosophila, are involved in male±male sperm competition, sexual
finally, showed that sympatric species have relatively stronger manipulation of females by males, and the female prevention
prezygotic isolation than allopatric species, which also lends of the latterÐa set of selective pressures referred to as
support to reinforcement as a relevant speciation mode in this sexually antagonistic selection.(60) Again, if males and females
group. do not coevolve (as in allopatric populations), their compat-
From the viewpoint of the isolation theory, then, these ibility will decrease, resulting eventually in both prezygotic and
recent data suggest that reinforcement can and does indeed postzygotic isolation.
produce new species. From the viewpoint of the selection All the situations mentioned above should result in a
theory, however, the relevance of reinforcement is reduced. situation where isolation is attained first, unrelated to environ-
As the process acts only on pairs of populations that are mental selection, after which the resultant genetic partitioning
already genetically and ecologically diverged and that have a would allow for independent adaptation in both daughter
strong (though not complete) degree of reproductive isolation, populations. Will the latter actually happen? Two facts make
it can be argued that reinforcement is not a speciation mode subsequent niche shifts unlikely in the ``instantaneous'' situa-
because it is not instrumental in the populations' divergence. tions. First, the reproductive isolation trait will usually be the
It only serves to reduce gene flow to zero. If the selection only genetic difference between populations that are incom-
viewpoint is adopted, reinforcement represents the same patible due to Wolbachia infection, coil reversal, or polyploidy.
phenomenon as reproductive character displacement: it is Second, the environment will remain unaltered. In coil reversal
adaptation within two populations that have already speciated. and Wolbachia infection, respectively, the conditions for the
establishment(61) and maintenance(15) of the isolation are
Redefining the role of reproductive isolation restrictive, and empirical evidence is rare.(54,58,62) Allopoly-
In the previous paragraphs, I have argued that the selection ploid (rather than autopolyploid) plants, however, are an
view may eventually be a preferable platform for discussing exception. The combination of two different genomes may
species and speciation than the isolation view. Selection, allow the new polyploid to be preadapted to a niche that is
rather than reproductive isolation, appears to be what drives intermediate between those of its parents. In fact, studies of
and keeps species apart, both in allopatric and in sympatric recently originated allopolyploids show that these establish
situations. It will be interesting, however, to examine in more successfully in such intermediate habitats (e.g., Tragopogon
detail the precise role of reproductive isolation, for two in North America see Refs. 63,64). Possibly, allopolyploid
reasons. (1) Models and observations exist where full pre- speciation may be a case where the isolation view is more
zygotic and/or postzygotic isolation evolves between popu- appropriate than the selection view. However, the same may
lations without any obvious environmental selection. (2) not be true for situations where isolation is attained through
Reproductive isolation is still important, as it will act as a sexual selection and/or sexually antagonistic selection.
catalyst of speciation processes that are initiated by selection. On the one hand, there is no doubt that speciation is often
Two types of ``non-environmental'' reproductive isolation, associated with strong divergence in traits for assortative
i.e., without any direct connection to environmental selection, mating and/or postzygotic isolation. For example, Odysseus, a
can be envisaged. First, there are situations of the ``instanta- gene responsible for hybrid male sterility between Drosophila
neous kind, where a single trait becomes fixed in a population, simulans and D. mauritiana has turned out to be a homeobox
rendering it reproductively isolated from other populations. gene, expressed in the testes, which evolves extremely rapidly
Examples include bidirectional cytoplasmic incompatibility due to an unknown selection pressure.(65,66) (See the article
in arthropods due to infection by the bacterial symbiont by Orr and Presgraves, this issue.) The fact that molecular
Wolbachia, as mentioned above,(14,15,54,55) coil reversal in phylogenies of the Drosophila simulans clade using this gene
globular snails, which causes mechanical incompatibility of show better resolution than those using other genetic markers,
the genitalia,(56± 58) and polyploidy in plants, which leads to suggests that it has been important in the speciation process
inviability of hybrids due to aneuploidy.(4) Second, recent from a very early stage onwards.(67) Many other genes in-
advances in the field of sexual selection suggest that isolated volved in reproduction show similar evidence for strong
populations can easily diverge in their systems for sexual selection, although usually it is not known if these genes are
signalling. Computer analysis of ``runaway'' sexual selection responsible for reproductive isolation between species.(68 ± 70)
has shown that this process exhibits unpredictable, cyclical Other evidence comes from comparative studies of speciation
behaviour, which is likely to run out of phase in allopatric rates in birds, which generally show that polygamous clades
populations.(59) This means that, soon after geographic (where ``runaway'' sexual selection will be more prevalent),
separation, male signals in one population may no longer show higher speciation rates.(71,72) In effect, sexual selection
coincide with a preference in females of the other population, can play a major role in incipient isolation.
leading to prezygotic isolation. Moreover, allopatric popula- On the other hand, however, sexual selection and sexually
tions are likely to diverge in the complicated sets of traits that antagonistic selection may often be chanelled by natural

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Box 1. Two concepts of speciation

``Isolation'' concept ``Selection'' concept

Speciation initiated by: Disruption of gene flow due to geographical, temporal, ecological, Adaptation to different environments
or any other type of gene-pool segregation; most rapid in
peripheral isolates, but also possible in other geographic settings
Speciation progresses by: Genetic drift and founder effects, natural selection or both Natural selection and superimposed sexual
selection
Speciation completed when: Pre- and/or postmating reproductive isolation has evolved Differently adapted gene pools have
evolved
Accompanying species Biological species concept Darwin's species definition
concept:
Geographic setting: Most rapid in peripheral isolates, but also possible in other Most-rapid in sympatry, but also possible in
geographic settings other geographic settings

selection. Colour variation in male guppies(73) and possibly natural selection. Reproductive isolation is then seen to take a
also cichlids,(74) for example, is influenced by the presence or catalytic, rather than an instrumental role. This view on species
absence of predatory birds, and mate selection in fishes is and speciation is surprisingly compatible with Darwin's ideas
often by body size, which is also an environmentally selected on the subject.
trait.(75) In addition, many types of reproductive isolation have Future work on the role of environmental selection should
been shown to be caused secondarily by environmental fill conspicuous gaps in our knowledge of speciation. The
selection. For example, flowering time in monkeyflowers has experiments by Kilias and co-workers(43) and Dodd,(44) which
diverged due to water regimes of the soil(76) and diurnal mating showed that prezygotic and weak postzygotic isolation
rhythms in melon flies have been shown to diverge as a evolved in ``allopatric'' laboratory populations of Drosophila
correlated response to larval development time.(77) Therefore, under conditions of different selection regimes, but not under
possibly, even in cases where species appear to have formed identical selection, urgently need a detailed follow-up. These
primarily due to the evolution of reproductive isolation, this studies indicate that reproductive isolation may often be a
reproductive isolation may have been actually superimposed by-product of selection, whereas theory(59,60) suggests that
on an underlying environmental selection. it might also build up independently. We may only have
In general, then, the role for reproductive isolation may be scratched the surface of the full extent of interactions between
seen as catalytic, rather than instrumental in speciation. The natural and sexual selection.
buildup of differently adapted gene pools will be disrupted by
recombination. Because assortative mating and postzygotic Acknowledgements
isolation can prevent this, selection and reproductive isolation For the development of the ideas presented in this paper, I am
are probably best viewed as mutually reinforcing, as has been indebted to several people who have helped shape my view-
pointed out by Rice and Hostert: once an initial episode of points, namely, John Endler, Jeffrey Feder, Arne Mooers, Bill
strong environmental selection causes partial reproductive Rice, Michael Rosenzweig, Ulrich Schliewen, Dolph Schluter,
isolation as a by-product, weaker selection (which otherwise and Chung-I Wu. The constructive comments by Jacques van
would have been hampered by gene flow) will then be able to Alphen, Jeroen Roelfsema, Jeffrey Feder, Ole Seehausen,
differentiate the two populations further, which in turn causes Chung-I Wu and two anonymous reviewers on an earlier
further reproductive isolation, and so on.(34) version of the manuscript are also gratefully acknowledged.
For the contents of this paper, however, only I am responsible.
Conclusions
In this paper, I have attempted to argue that many of the References
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BioEssays 22.12 1141

121
122
MÓDULO VII:

EVOLUCIÓN 
Y

DESARROLLO
(EVO­DEVO)

123
124
  TRABAJOS PRÁCTICOS 

 EVOLUCIÓN Y DESARROLLO (EVO­DEVO) 

Por Nicolás Frankel

“Evolution occurs when ontogeny is altered in one of two ways: when new characters are 
introduced at any stage of development with varying effects upon subsequent stages, or when 
characters already present undergo changes in developmental timing” 
S.J.Gould en “Ontogeny and Phylogeny” (1977)

BREVE INTRODUCCIÓN

El término “evolución” fue usado por los preformacionistas del siglo XVIII para 
describir  el  proceso  por  el   cual   un  embrión  crece   hasta   convertirse  en  un   organismo 
adulto. Esta es la primera connotación biológica del término y difiere claramente de su 
significado actual. Los preformacionistas creían que el embrión estaba ya ubicado dentro 
de la célula germinal con todas sus partes ya formadas y simplemente crecía en tamaño 
hasta  alcanzar el estado adulto. El ejemplo extremo de este punto de vista es el del 
homúnculo,   el   hombrecito   con   proporciones   de   adulto   dibujado   dentro   del   esperma. 
Malpighi  y Bonnet  (ambos representantes  del  Preformacionismo) habían estudiado el 
desarrollo   del   embrión   de   pollo   y   conocían   el   aumento   de   complejidad   aparente   al 
microscopio (poco coherente con las ideas preformacionistas). A pesar de ello afirmaban 
que lo que veían era ilusorio y estaba sesgado por los instrumentos usados y los sentidos. 
En el siglo XIX, con el nacimiento de la Embriología comparada, comienzan a oírse 
otras   voces   que   hablan   del   desarrollo.   Ètienne   Geoffroy   Saint­Hilaire   sugiere   que   la 
homología de una estructura puede ser inferida por las relaciones con otras estructuras 
durante el desarrollo embrionario. A diferencia de Cuvier, que dividía los animales en 
cinco clases sin relación entre sí, Geoffroy sostenía que todos los animales compartían 
grandes similitudes en su anatomía. 
En el mismo siglo, Haeckel expone su visión recapitulacionista. Considera que la 
filogenia   es   la   que   determina   la   ontogenia,   ya   que   los   animales   pasan   durante   su 
desarrollo   por   las   formas   adultas   de   otras   especies   “inferiores”.   El   cigoto   humano 
representa al protista adulto, la blástula humana representa a los protistas coloniales, el 
estadio humano de arcos branquiales al pez adulto, etc. Las nuevas especies evolucionan 
adicionando   un   paso   más   en   el   desarrollo.   Igualmente,   Haeckel   manifiesta   que   es 
factible un acortamiento del desarrollo en algún tramo para evitar un infinito tiempo de 
gestación. En 1828, Karl Ernst Von Baer enuncia algunos puntos importantes en sus 
leyes del desarrollo:
1. Las características generales de un gran grupo de animales aparecen antes en 
el embrión que las características particulares de un grupo menor.
2. Los animales no pasan durante su desarrollo a través de formas adultas de 
otros organismos “inferiores” (contradice a los recapitulacionistas).
3.   Los   embriones   de   especies   emparentadas   comparten   estadios   tempranos   de 
desarrollo pero divergen en los estadios más tardíos.

125
 4.   Los   caracteres   más   especializados   se   desarrollan   a   partir   de   estructuras 
generales compartidas por distintas especies.

El trabajo de Von Baer influyó fuertemente en el pensamiento de Darwin, quien 
consideró   las   similitudes   en   el   desarrollo   de   distintas   especies   como   evidencia   de 
ancestralidad   común.   Fritz   Müller   (un   acérrimo   defensor   del   Darwinismo)   y   Francis 
Balfour   resaltan   en   sus   escritos   la   importancia   de   la   Embriología   Comparada   como 
herramienta   para   dilucidar   las   relaciones   filogenéticos.   Afirman   también,   que   la 
selección natural debe actuar tanto en los estadios larvales como en los adultos. 
En el siglo XX, el advenimiento de la “Teoría Sintética de la Evolución” acerca la 
Genética a la Evolución en detrimento de la Biología del Desarrollo. Esta última es uno 
de   los   capítulos   faltantes   en   la   “Síntesis”.   Las   causas   de   esta   importante   ausencia 
pueden   haber   sido   muchas,   pero   la   más   importante   parecería   ser   la   falta   de 
entendimiento   entre   genetistas   de   poblaciones   y   embriólogos.   En   los   ‘40s   Richard 
Goldschmidt, sostiene que la evolución puede ocurrir sólo por cambios heredables en los 
genes que regulan el desarrollo. Para él los genes son más que loci y alelos, son unidades 
de desarrollo. Las nuevas especies se originan como “monstruos esperanzados” (“hopeful  
monsters”) que resultan de mutaciones  sistémicas  que afectan el desarrollo del animal. 
Su visión, al ser contraria a la neo­darwinista, no es tenida en cuenta en su  época. En 
1977,   Stephen   Jay   Gould,   publica   el   libro  Ontogeny   and   Phylogeny  y   reaviva   en   el 
ambiente   científico   el   interés   por   la   Biología   del   Desarrollo   como   herramienta   para 
estudiar la evolución. 
En 1978, E.B. Lewis descubre los genes  Hox  (los encargados de dar identidad a 
cada   parte   del   animal   a   lo   largo   del   eje   antero­posterior)   y   unos   años   más   tarde 
comienza   a   conocerse   en   profundidad   el   desarrollo   embriológico   de  Drosophila  
melanogaster, Caenorhabditis elegans y del ratón. Paralelamente, la Biología Molecular 
avanza   a  pasos   agigantados  y   provee  nuevas   herramientas   de  análisis.  Estos   hechos 
recientes marcan el comienzo de la Evo­Devo moderna. 
En   la   actualidad   la   interfase   entre   Evolución   y   Desarrollo   atraviesa   un 
renacimiento. En él convergen disciplinas como la Biología del Desarrollo, la Ecología, la 
Embriología, la Paleontología, la Genómica y el Análisis Filogenético. Esta combinación 
de enfoques y metodologías tiene como objetivo desentrañar los mecanismos y patrones 
del   desarrollo  que  originan   la   diversidad  de  formas   vivientes   que  existen   en  nuestro 
planeta.
En   este   momento   existen   dos   revistas   científicas   cuyos   artículos   tratan 
exclusivamente   temas   de   Evolución   y   Desarrollo;   estas   son:   “Evolution   and 
Development” y “Development, Genes and Evolution”.

126
BIBLIOGRAFÍA CONSULTADA

Carroll S.B., Grenier J.K. and Weatherbee S.D. 2005. From DNA to diversity, Second 
Edition. Blackwell Publishing.
Gilbert S.F. 2003. Developmental Biology, 7th Edition. Sinauer Associates.
Gilbert   S.F.   2003.   The   morphogenesis   of   evolutionary   developmental   biology. 
Int.J.Dev.Biol. 47(7­8):467­77.
Gould S.J. 1977. Ontogeny and Phylogeny. Belknap Press of Harvard University Press.
Hall   B.K.   2003.   Evo­Devo:   evolutionary   developmental   mechanisms.  Int.J.Dev.Biol. 
47(7­8):491­5.
Wilkins A.S.2002. The evolution of developmental pathways. Sinauer Associates.

127
 TRABAJO PRÁCTICO 1 : SEMINARIO

Lea atentamente los siguientes trabajos y responda las preguntas:

1.  Gerhing,   W.J.   &   Ikeo,   J.   1999.  PAX   6:   Mastering   eye   morphogenesis   and   eye 
evolution. TIG 5(9):473­479.
1.1.  Comente   las   dos   hipótesis   sobre   el   origen   y   evolución   del   ojo.   Utilice   el 
ejemplo de Arca, Cardium y Pecten para ilustrar estas dos hipótesis.
1.2.  Nombre   las   evidencias   que   sustentan   a   Pax6   como   un   gen   maestro   en   el 
desarrollo de los distintos ojos de los animales.
1.3. Según los autores la universalidad de dos importantes componentes del ojo de 
los metazoos como son Pax6 y la rodopsina sugiere fuertemente la existencia de 
un   proto­ojo   y   por   lo   tanto   la   monofilia   de   esta   estructura.   Nilsson   (Current  
Biology  15: R94­R95 (2005)) critica esta idea porque no tiene en cuenta que los 
ojos   de   insectos   y   vertebrados   tienen   distintos   orígenes   embriológicos   y   usan 
distintos tipos de células fotorreceptoras para la visión (células rabdoméricas en 
insectos y células ciliadas en vertebrados). 
¿Qué opina ud.? Muchas veces las definiciones no permiten la existencia de grises. 
¿Pueden ser los ojos de los metazoos parcialmente homólogos?
1.4. Analice la figura 4, ¿qué plantea la idea de “intercalary evolution”?
1.5. Gehring e Ikeo sugieren que el proto­ojo pudo haber surgido por azar. Si los 
autores estuviesen equivocados y el ojo surge a partir una estructura que tiene la 
capacidad de sensar  la  luz  pero  no es  un  ojo propiamente dicho (no  tiene una  
célula fotorreceptora y una célula pigmentada) ¿Cuál podría ser la función de esta 
estructura ancestral?
1.6.  En un trabajo reciente (Arendt et al. 2004  Science  306:869­871) se descubre 
que   el   anélido   Platynereis   (que   supuestamente   conserva   características   del 
ancestro de los animales bilaterales) tiene células rabdoméricas y células ciliadas 
asociadas a la fotopercepción. ¿Qué le sugiere este hallazgo? Recuerde los tipos de 
fotorreceptores (pregunta 3) que usan vertebrados e insectos.

2. Wagner, G.P. 2007. The Developmental genetics of homology. Nat.Genet. 8:473­479.

2.1. ¿Cuál es la base del concepto de homología empleado por el autor para genes y 
caracteres morfológicos?
2.2. Analice las implicancias de la figura 2.
2.3. ¿Qué analogías propone el autor entre genes y caracteres morfológicos?
2.4. ¿Qué propone acerca de las redes genéticas regulatorias (GRN)? ¿Cómo se 
relacionan con las redes de identidad de caracteres (ChIN)?

128
 2.5. ¿Cuál, y de qué tipo, es la relación de homología entre: alas delanteras, alas 
posteriores, élitros y halterios? ¿Qué ChIN estaría involucrado? ¿Cómo?
2.6. Explique la morfogénesis del ojo en vertebrados y en Drosophila. Compare 
con la propuesta de Gehring e Ikeo. Indique las hipótesis propuestas para explicar 
las diferencias.

3.  Galis,   F.   1999.   Why   do   almost   all   mammals   have   seven   cervical   vertebrae? 
Developmental constraints, Hox genes and cancer. J.Exp.Zool. 285:9­26.
3.1.  ¿Cuál es la restricción (constraint) al cambio sobre la que versa el trabajo? 
¿Existe variación intraespecífica del número de vértebras en las distintas regiones 
de la columna de los mamíferos?
3.2.  ¿Qué distingue una vértebra torácica de una cervical? ¿Qué es una costilla 
cervical? ¿Cuáles son las patologías asociadas con las costillas cervicales?
3.3.  ¿Cuál   es   la   función   conservada   de  los   genes   Hox   en  animales   bilaterales? 
¿Qué patologías tienen los ratones mutantes de algunos genes Hox o Polycomb?
3.4. La restricción al cambio en el número de vértebras cervicales: ¿está dada por 
ausencia de variación para ese carácter o por selección en contra de variantes de 
ese carácter? ¿Cómo se presenta en humanos la selección estabilizadora?
3.5.  ¿Cuál   es   la   conclusión   del   autor   en   cuanto   a   la   relación   entre   el   número 
conservado de vértebras cervicales en mamíferos, el cáncer y los genes Hox? ¿Por 
qué esta relación no se presentaría en reptiles y anfibios?

129
Eye morphogenesis and evolution Perspectives

Pax 6
mastering eye morphogenesis
and eye evolution
Pax 6 genes from various animal phyla are capable of inducing ectopic eye development, indicating that Pax 6
is a master control gene for eye morphogenesis. It is proposed that the various eye-types found in metazoa are
derived from a common prototype, monophyletically, by a mechanism called intercalary evolution.

xplaining the evolution of an organ as perfect as the eye scallop, Pecten), and compound eyes that consist of 10–80
E is a great challenge for all evolutionary biologists. In his
theory ‘The Origin of Species’ Charles Darwin devoted an
ommatidia each (in Noah’s arc, Arca noae)], are found in
the same phylogenetic class, the Bivalvia (Fig. 1). All of
entire chapter to the problem. Darwin freely admitted that these types of eye are located at the same anatomical pos-
the idea of an eye that is capable of adjusting the focus to ition – the edge of the mantle. The compound eyes of Arca
different distances, of admitting different amounts of light are similar to those of arthropods, but they have only a sin-
and of correcting spherical and chromatic aberration, could gle photoreceptor cell per ommatidium, whereas insects and
have been formed by natural selection seems intuitively crustaceans generally have eight or nine visual cells per unit.
absurd. However, he subsequently found a way out of this Salvini-Plawen and Mayr interpret the compound eyes of
dilemma by postulating a simple and imperfect eye, a proto- Arca as new formations, but an equally valid interpretation
type, from which the more perfect visual organs might have of these data is to assume that the camera-, mirror- and
arisen gradually, by variation (mutation) and by natural compound eyes of clams have evolved monophyletically
selection. Darwin assumed the prototype to consist of at from a common ancestral precursor. A monophyletic origin
least two cells: an ‘optic nerve’ (photoreceptor cell) and a for the eye is also supported by the observation that all
pigment cell shielding the photoreceptor cell from one side, metazoans share the same visual pigment, rhodopsin.
covered by translucent skin, but without any lens or other Darwin was highly self-critical in his discussion of the
refractive body. Such primitive eyes are found, for example, eye prototype and admits that the origin of the prototype
in some planarians (Fig. 1). Comparative anatomists have cannot be explained by natural selection, because selection
discovered numerous intermediates between this most primi- can only drive the evolution of an eye once it is partly
tive type of eye and the vertebrate eye, such as: eye cups; functional and capable of light detection. Therefore, selec-
pinhole eyes; camera-type eyes with a single lens; reflecting tion cannot explain the origin of the eye prototype, which
mirror eyes; and compound eyes with numerous ommatidia, for Darwin represents the same problem as the origin of
all of which lends support to Darwin’s theory. life. Therefore, both the origin of life and the origin of the
On the basis of comparative anatomical and ultrastruc- eye prototype must have been very rare events, and a poly-
tural studies of the various types of eye and photoreceptor phyletic origin in over 40 different phyla is not compatible
cells, it has been postulated by Salvini-Plawen and Mayr1, with Darwin’s theory. In this review, we discuss more
two strong proponents of darwinism, that photoreceptor recent evidence in favor of a monophyletic origin of the
organs have originated independently in at least 40, but eye and propose a new hypothesis explaining how
possibly up to 65 or more different phyletic lines. However, morphogenetic pathways might have evolved. Walter J. Gehring
there are some critical facts that are not consistent with this gehring@
conclusion, and we would like to challenge this idea and Pax 6 is a master control gene for eye ubaclu.unibas.ch
argue for a monophyletic rather than a polyphyletic origin morphogenesis and evolution *Kazuho Ikeo
of the metazoan eye. Salvini-Plawen and Mayr argue purely Homeotic mutations in Drosophila have resulted in the kikeo@genes.nig.ac.jp
on morphological grounds. Their section on ‘the multiple identification of several master control genes that specify
origin of eyes’ begins with the comment that ‘it requires lit- the body plan by controlling anterior–posterior polarity, Department of Cell
tle persuasion to become convinced that the lens eye of a segmental identity, organogenesis and identity of individ- Biology, Biozentrum,
vertebrate and the compound eye of an insect are indepen- University of Basel,
ual cells in great detail. The term ‘master control genes’
Klingelbergstrasse 70,
dent evolutionary developments’. This point has been was introduced by Lewis2 for the homeotic genes of the
4056 Basel, Switzerland.
taught to biology students for over a hundred years. Bithorax Complex, and, perhaps the most impressive *Center for Information
However, in a later section (p. 237) these authors describe demonstration of their role in development has been the Biology, National
the observation that, in clams, all three major eye-types [the genetic construction of four-winged and eight-legged flies3. Institute of Genetics,
camera eye with a single lens (in the heart shell, Cardium), Targeted expression of the homeotic Antennapedia gene Mishima,
the mirror eye with a lens and a reflecting mirror (in the results in complete middle legs being induced in the antennal Yata 411, Japan.

0168-9525/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved. PII: S0168-9525(99)01776-X TIG September 1999, volume 15, No. 9 371

130
Perspective Eye morphogenesis and evolution

FIGURE 1. Eye evolution

A hypothetical scheme of the evolution of various eye-types from a common ancestral prototype. As a first step, photosensitive cells with a light receptor (opsin)
have evolved. Under the control of the Pax 6 gene, the photosensitive cell assembles with a pigment cell to form an organ, the prototype eye. By divergent, parallel
and convergent evolution, the various eye-types are generated from the prototype: the compound eye of insects; the camera-type eye of vertebrates; and the large
spectrum of eye-types in molluscs ranging from the primitive camera-type eye in Cardium, the mirror-plus-lens eye of Pecten, the compound eye of Arca to the highly
evolved cephalopod eye, that greatly resembles the vertebrate camera-type eye.

discs of Drosophila3. Another striking example of a master course of evolution by recombining parts of pre-existing
control gene is Pax 6. This gene was first cloned in the genes in a process that Jacob called evolutionary tinkering7.
mouse4,5 and in humans6 and subsequently shown to be The different Pax genes contain various combinations of
affected in the mouse mutant, Small eye, and in human paired domains, with homeodomains, a sequence called
Aniridia patients. In humans and mice, eye defects are as- octapeptide, or parts of the homeodomain and paired
sociated with Pax 6 mutations in heterozygotes. The domain, respectively. The murine and human PAX 6 pro-
homozygous Pax 6 mutation is lethal to mouse embryos: teins are identical in amino acid sequence. A Pax 6 homolog
they lack eyes and a nose, and also have brain damage. Pax in Drosophila8 was subsequently discovered and this also
6 is expressed from the earliest stages of eye morphogenesis shows extensive sequence similarity, both in the paired
in the optic vesicle, giving rise to the retina and pigment domain (94% identity), and in the homeodomain (90%
retina, as well as in the overlying ectoderm that later forms identity). More surprising is the finding that the Drosophila
the lens and the cornea. However, Pax 6 is also expressed Pax 6 homolog is the eyeless (ey) gene known by a mutation
in the nasal epithelium, in specific regions of the brain and affecting the eyes since 1915 (Ref. 9). This was unexpected
the spinal cord, and not exclusively in eye primordia. because of the long-standing dogma, mentioned above, that
Pax 6 encodes a transcription factor that contains a the insect compound eye was non-homologous to the verte-
paired domain and a homeodomain. The Pax gene family brate camera eye, and that the two types of eye had evolved
clearly illustrates that novel genes are generated in the independently. The observation that Pax 6 homologs of

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Eye morphogenesis and evolution Perspectives

both mammals and insects are essential for eye morpho- Genuine Pax 6 genes have now been isolated from:
genesis led to the idea that Pax 6 might be the universal mammals; amphibians; fish; amphioxus; sea squirts; sea
master control gene for eye morphogenesis and evolution8. urchins; squid; nematodes; ribbonworms; and planarians
We tested the master control gene hypothesis by con- (Fig. 2). In Cnidarians the situation is less clear, because the
structing a gain-of-function mutation. In wild-type larvae, genes found so far are either precursors of Pax 6 or have
ey is expressed exclusively in the eye-antennal disc from the diverged too far to be clearly identified as Pax 6 homologs.
earliest stages when the disc primordia are formed in the In any case, this survey shows that Pax 6 was present in the
embryo. Therefore, we used the Gal-4-system to target gene last common ancestor of all these triploblastic phyla, much
expression into imaginal discs other than eye discs10. By the like the rhodopsin gene. In addition to the mammalian Pax
use of different genomic enhancer lines, we were able to 6 gene, its homologs from the sea squirt Phallusia and the
induce ectopic eyes on the legs, wings, halteres and the squid Loligo are also capable of inducing ectopic eyes in
antennae of the fly, and recent electrophysiological exper- Drosophila. With the exception of sea urchins and
iments show that the ectopic eyes on the antenna can gener- Caenorhabditis elegans (which presumably have lost their
ate a normal electroretinogramme, which indicates that eyes during evolution because eyes are found in other echino-
they are functional (P. Callaerts and W. Gehring, unpub- derms and nematodes), all Pax 6 genes examined so far are
lished). This illustrates the role of ey as a master control expressed prominently in the developing eyes, including
gene that is capable of switching on a cascade of some 2500 those of planarians, which come close to the darwinian
genes required for eye morphogenesis10. Of course, eye prototype. Furthermore, Pax 6 is specifically expressed in
morphogenesis cannot be induced in any tissue of the fly the differentiated eyes of the ribbonworm Lineus14 and par-
at any stage of development, but at least it does occur in ticularly during eye regeneration15, strengthening the corre-
all imaginal discs up to a certain stage of differentiation. lation between eye morphogenesis and Pax 6 expression.
The master control gene first has to interact with subordi-
nate control genes to repress the resident genetic pro- The evolution of Pax 6: twin of eyeless
gramme and to install the eye programme. If the cells have More recently, a second Pax 6 gene homolog in
proceeded too far along their pathways and are firmly Drosophila called twin of eyeless (toy) was identified16. It
locked into a different pathway, the ectopic expression of ey shares 91% sequence identity in the paired domain and
has no effect. 90% in the homeodomain with the human and murine
Our next query was whether the mammalian Pax 6 PAX 6 proteins (Fig. 2), compared with 95% and 90% for
gene can functionally substitute for the Drosophila EY. Outside of these highly conserved domains, TOY is
homolog. The ectopic expression of mouse Pax 6 in more similar to the mammalian proteins than EY, particu-
Drosophila induces ectopic compound eyes10, suggesting larly in its overall length and at the C-terminus, where it
that Pax 6 has a universal function of gene regulation in shares a transcriptional activation domain with other PAX
eye morphogenesis. The reciprocal experiment has not 6 proteins that is absent in EY. A survey by polymerase
been completed yet, but it has been reported that Xenopus chain reaction (PCR) shows that two Pax 6 genes are only
Pax 6 is capable of inducing ectopic eye lenses11. However, found in holometabolous insects (Drosophila and
by changing the timing and site of Pax 6 RNA injection Bombyx) and not in hemimetabolous (grasshopper) or
into the Xenopus embryo, it is possible to induce complete apterygote insects (springtail), nor in all other phyla
ectopic eyes (R. Chow, C. Altmann, R. Lang and tested16. This indicates that the gene-duplication event
A. Hemmati-Brivanlou, pers. commun.). These findings leading to the two paralogs occurred during insect evolu-
clearly indicate that Pax 6 is a master control gene for eye tion, a conclusion that is also supported by the molecular
morphogenesis in both insects and vertebrates. phylogenetic analysis (Fig. 3). Besides the sequence simi-
The protein-coding regions of Pax 6 are highly con- larity, the localization of the intron splice sites clearly indi-
served in evolution, as are some of the regulatory cates that both paralogs are bona fide Pax 6 genes (Fig. 2).
sequences in the promoters and enhancers. Consequently, The first splice site at the N-terminus of the paired domain
the regulatory mechanisms that direct ocular expression is missing in toy, but present in ey, whereas the second
are also conserved between flies and mice. The eye-specific splice site in the homeodomain is present in toy and absent
enhancer region of the Drosophila ey gene8,12, when in ey, indicating that the ancestral gene had all four splice
inserted upstream of either of the two mouse Pax 6 pro- sites in the two boxes. The same four splice sites are also
moters (P1 or P0), directs eye- and CNS-specific expres- found in the nematode Caenorhabditis elegans and three
sion in transgenic mice that accurately reproduces features out of four can be traced back to platyhelminths
of endogenous Pax 6 expression13. In a reciprocal exper- (Dugesia). This indicates that these introns are very old
iment, the mouse P1 element is able to direct lacZ reporter (precambrian) and that a bona fide Pax 6 gene must have
gene expression into the eye imaginal discs of Drosophila. been present in the last common ancestor of triploblastic
Here, the expression is restricted to the photoreceptor animals. Vertebrates share a splice site at codon 44/45 that
cells, although lacZ expression is delayed and occurs only is vertebrate-specific and is used for differential splicing in
posterior to the morphogenetic furrow, whereas endogen- the paired box. It is absent in amphioxus and ascidians,
ous ey expression is confined to the undifferentiated cells indicating that this intron arose later in evolution, after
anterior to the morphogenetic furrow. However, the vertebrates had separated from invertebrates.
Drosophila ey enhancer itself shows the same spatio– Following gene duplication during insect evolution, the
temporal expression pattern as the mouse promotor, two paralogs ey and toy began to diverge in function. In
that could reflect perdurance of b-galactosidase or lack particular, toy is expressed much earlier, at the blastoderm
of regulatory sequences that confer repression posterior to stage, when the Drosophila body plan is laid down,
the morphogenetic furrow12. Overall, there is evidence whereas ey is expressed only later, during germband
for conservation of Pax 6 gene regulation, but there is extension. The spatial patterns at later stages are very
uncertainty about the extent of the conservation. similar although not identical. This earlier divergence with

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Perspectives Eye morphogenesis and evolution

FIGURE 2. Metazoan Pax 6 proteins

(a) b1 b2 a1 a2 a3

1 10 20 30 40 50 60 70

Homo, Mus SHSGVNQLGGVFVNGRPLPDSTRQKIVELAHSGARPCDISRILQVSNGCVSKILGRYYETGSIRPRAIGGSKPRVA

Amphioxus G............G.........R.......Q.........L..................................
Phallusia G.........M..........I......F..N......................A......T..............
Paracentrotus G...........................................................................
Loligo G.......................R...................................................
Lineus G.......................R.........................T.........................
Drosophila EY G............G..............................................................
Drosophila TOY G...I......Y...................................................K............
Caenorhabditis G.T.................A...R..D...K.C.......L............C....S.T..............
Dugesia G . . . I . . . . . I . . . . . . . . . V . . . R . I . . S Q . . . . . ..................C........K.K..........
..................C........K.K..........

Hydra (B) N.G.I.....T.......IEPV.R.......Q.V.......Q.R..H.......S.F.....V...V......K..

Pax4 L.S......L........LD...Q..Q..IR.M.......S.K..............R..VLE.KC.......L.
Pax2 R.G.................VV..R......Q.V.......Q.R..H................K.GV......K..
Pax5 G.G.................VV..R......Q.V.......Q.R..H................K.GV......K..
Pax8 G.G.L.....A........EVV..R..D...Q.V.......Q.R..H..................GV......K..

a4 a5 a6

80 90 100 110 120 130

Homo, Mus TPEVVSKIAQYKRECPSIFAWEIRDRLLSEGVCTNDNIPSVSSINRVLRNLASEKQQMGADG---MYDKLRMLNGQ 100

Amphioxus . . . . . A . . . . F . . . . . . . . . . . . . . . . . . . . I . . . E . . . . . . . . . . . . . . . . . G E K N T L - ( X )9 - . L E . . . L . . . N 92
Phallusia ..Q..N...M..................N.A..NAE...............NG.NGRVFSEGNSPNKNHLPDDWSS 87
Paracentrotus ..H..TR..H..................A.KI.NQE...................TMGHGD----.F......... 91
Loligo .....Q....F.......................Q.................G.N.KVLGQ.-TTT....GL.... 96
Lineus .....G...H...................DA..NQ...................N.KQLGQSS--.....GL.... 93
Drosophila EY . A . . . . . . S . . . . . . . . . . . . . . . . . . . Q . N . . . . . . . . . . . . . . . . . . . . . A Q . E . Q S - ( X )70 - I . E . . . L . . T . 95
Drosophila TOY .TP..Q...D....................Q..NS..................Q.E.QAQQQNESV.E....F... 91
Caenorhabditis .SD..E..ED...DQ..........K..ADNI.N.ET...............AK.E.VTMQTE--L..RI.IVDNF 80
Dugesia .NT..R.VTI..Q.S..M........P.QD...NQ..L..I.....I..S..N.SPSSNQTFKSSLSNSHQLSLSN 77

Hydra (B) ..S..A..QE..QHN.TM.......K....QI.DS.SV........IV..RLGS 68

Pax4 ..A..AR...L.D.Y.AL.....QHQ.CT..L..Q.KA...........A.QED 70
Pax2 ..K..D...E...QN.TM..........A..I.D..TV........II.TKVQQ 77
Pax5 ..K..E...E...QN.TM..........A.R..D..TV........II.TKVQQ 77
Pax8 ..K..E..GD...QN.TM..........A....D..TV........II.TKVQQ 75

(b) a1 a2 a3 / 4

1 10 20 30 40 50 60

Homo, Mus DEAQMRLQLKRKLQRNRTSFTQEQIEALEKEFERTHYPDVFARERLAAKIDLPEARIQVWFSNRRAKWRREEKLRNQRR 100

Amphioxus ....A..R....................................................................... 100
Phallusia KDTNA...............S...V......................S.........................M.H..G 95
Paracentrotus ED..A..R.............AQ...E....................Q............................... 93
Loligo TDE...IR.............AA.......G................HQ............................P. 92
Lineus S.E...IR.............NA........................Q............................... 93
Drosophila EY EDD.A..I.............ND..DS....................G..G............................ 90
Drosophila TOY EDS....R............SN...DS....................D..G......................M.T... 90
Caenorhabditis .D.AA.MR..............V...S....................Q..Q......................M..K.S 93
Dugesia RYSNTESK.SK.S..S.....ND..NL..............S..K.SQNLKVA.T..................SEENNM 73

Hydra (B) MR.V..T.SL..RR...DA..K.P...AEQ..EISIQC....P.V......K...L..QD 55

Pax4 SH...AI.SPG.A.......Q.GQ...SV..GK...ATS...DTVR............Q. 62
Pax2 ...Q.L...DRV...PS.....
Pax5 ...Q.L.V.DRV...Q..S.I.
Pax8 .S.HHL....CP...Q...EAY trends in genetics

Comparison of the amino acid sequences for PAX 6 proteins from various metazoa. The paired domains are indicated in (a) and the homeodomains in (b). PAX 6
protein-specific amino acids are shaded more darkly. The positions of the intron splice sites are indicated by arrowheads. These have not yet been determined for
Amphioxus, Paracentrotus and Loligo. The numbers indicate the percentage amino acid sequence identity as compared with the mouse and human proteins. For
comparison the closely related Pax sequences from the mouse (m) are shown. Pax 2, 5 and 8 have only partial homeodomains. a, a-helices; b, b-sheets.

respect to temporal rather than spatial patterns of gene mental pathway18 by directly regulating the eye-specific
expression has been found in other duplicated develop- enhancer of the ey gene12,16. This observation reveals
mental control genes, like sloppy-paired 1 and 2 (Ref. 17), an interesting facet of the evolution of morphogenetic
and might be a more general feature of evolution. Like ey, pathways: the single Pax 6 in vertebrates is autoregulated
toy is also capable of inducing ectopic eyes in Drosophila, by a positive feedback loop in which the PAX 6 protein
but toy requires a functional ey gene to induce eyes, binds to the enhancer in its own gene and activates its
suggesting that toy is upstream of ey in the genetic cascade transcription19. In Drosophila, after gene duplication
controlling eye morphogenesis. Epistasis experiments, as this positive autocatalytic feedback loop appears to
well as biochemical and transgenic analyses, support the have evolved into a heterocatalytic loop in which
notion that toy acts upstream of ey in the eye develop- one of the paralogs regulates the other, leading to the

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Eye morphogenesis and evolution Perspectives

integration of ey into the eye developmental pathway genes interact. It has been proposed that the two protein
underneath toy. products can form a heterodimer, which is compatible
with the findings mentioned above30.
The genetic cascade specifying the eye One of our aims is to compare the genetic cascade from
developmental pathway Drosophila with that of the mouse or other vertebrates to
Following the discovery of ey as a master control gene, find out how many other genes besides Pax 6 and the
several groups have embarked upon the analysis of the rhodopsin gene have been conserved during evolution.
genetic cascade leading to eye morphogenesis by identifying Several homologs for so and eya have been identified in ver-
target genes and genetic interactions. However, the direct tebrates, and a second so-like gene has also been isolated
nature of a given genetic interaction and the molecular basis from Drosophila31. However, sequence conservation of the
of the interaction has been demonstrated in only a few protein-coding region does not necessarily imply that the
cases. In Drosophila, evidence for a direct activation of ey function in eye morphogenesis is also conserved in evolution.
transcription by binding of TOY protein to the eye-specific For example, the mouse Rx gene that belongs to the paired-
enhancer of the ey gene has been described above. This puts like class of homeobox genes was shown to be expressed
the toy gene on top of the hierarchy and ey underneath16. both in the developing retina and forebrain. Loss-of-function
The toy gene requires ey to induce eye formation; in turn, ey mutants in mice do not form optic cups and, as a conse-
induces and requires sine oculis (so) and eyes absent (eya) quence, lack eyes32. Furthermore, misexpression of Rx
for the induction of ectopic eyes18. There is strong evidence induces ectopic retinal tissue in frogs32. However, a
that so is a direct target for EY protein20. However, as more Drosophila homolog of Rx that has 100% sequence identity
and more pieces are filled into the puzzle, the simple linear in the homeodomain is expressed only in the developing
pathways turn into a complex network and several other brain, but not in the embryonic or the larval eye primordia33.
genes have been found to be capable of ectopic eye induc- Eventually, it will be interesting to find how many new genes
tion. The so gene encodes a homeodomain protein that is must be recruited into the eye-developmental pathway to
required for the development of the entire visual system in generate either a mouse or a Drosophila eye, and how many
Drosophila21,22. The eya gene encodes a novel type of of these genes are common. However, the major changes
nuclear protein involved in the development of the visual occurring during evolution are likely to occur at the level of
system as well as in the somatic gonadal precursors23,24. gene regulation, and very different types of eye might be
A gene called dachshund (dac) encodes a novel nuclear generated by the same set of regulatory genes.
protein that is required for differentiation of the ommatidia,
but is also essential for leg development25,26. The ectopic The evolution of the different types of eye
expression of eya or dac alone or in combinations of eya The evolution of light-sensitive cells is intimately con-
with so or dac induces ectopic eye formation, but also nected to the evolution of the visual pigment rhodopsin.
activates ey expression. The ey, eya and dac genes are all Rhodopsin is the molecule of ultimate sensitivity because
activated during eye induction18 and there is evidence that it is capable of sensing a single light quantum. Absorption
the EYA protein forms a complex with SO (Ref. 27) and of a single quantum of light converts all-trans retinal, that
DAC (Ref. 28) proteins. Taken together, these findings can is covalently bound to the opsin protein molecule, into
be explained by a model in which ey induces the initial 11-cis retinal. This conversion causes a conformational
expression of so and eya that regulates the activity of all change of the protein that is amplified by transducin, a
four genes by positive feedback loops required for eye G-protein and results in an electrical nerve impulse34.
induction16.
Targeted expression of the gene teashirt (tsh), which
was shown to be required for the specification of the trunk
segments in the Drosophila embryo, can also induce FIGURE 3. Phylogenetic tree of the Pax 6 genes
ectopic eyes29. This gene encodes a transcription factor Dugesia
with zinc-finger motifs and induces the expression of ey,
Caenorhabditis elegans
so and dac. In turn, ey induces the expression of tsh, indi-
cating that tsh is also a member of the regulatory network Phallusia
toy
of genes that are connected to each other by positive feed- Drosophila melanogaster
back loops. However, it should be emphasized that ey is a eyeless
much more potent inducer of ectopic eyes than any single squid
gene in the later group, suggesting that no single gene can ribbon worm
recapitulate the entire spectrum of ey activity, reinforcing sea urchin
the master control gene status of Pax 6. amphioxus
A second Pax gene, eyegone (eyg) apparently acts in medaka fish
parallel with ey in determining Drosophila eye develop- zebrafish
ment30. This gene contains only a partial paired domain, Xenopus laevis
but a complete homeodomain. Loss-of-function mutations 0.05
quail
lead to a reduction of the eyes similar to ey, and ectopic
mouse
expression leads to the induction of ectopic eyes. The two
genes eyg and ey seem to have complementary functions human trends in genetics

because their coexpression leads to a synergistic enhance-

ment of ectopic eye formation. The expression of eyg is The neighbor-joining method was used to generate a phylogenic tree of the Pax 6 genes from various
metazoa. Note that Drosophila melanogaster eyeless and twin of eyeless are closely related. The scale
not regulated by ey at the transcriptional level, nor does it
shows the number of amino acid substitutions per site. The monophyly of the eyeless/Pax 6 group of
regulate ey expression. However, homozygous ey:eyg genes is strongly supported by the phylogenetic analysis of Jacobs et al.42
double mutants are lethal, which indicates that the two

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Perspectives Eye morphogenesis and evolution

Rhodopsins are present in some bacteria, and some of brates and invertebrates analyzed so far, typical rhodopsins
these proteins also serve a sensory function. However, belonging to one and the same gene family have been found.
there is very little sequence conservation between bacterio- The visual system of unicellular organisms is an organelle,
rhodopsins and rhodopsins of higher organisms, even rather than an organ, and it is formed by intracellular
though both are structurally similar membrane proteins assembly processes, whereas the eyes of metazoa are organs
with seven transmembrane domains. made up of cells of at least two different types or of different
Protists have also developed visual systems that are based tissues, as already pointed out by Darwin. There is accu-
on rhodopsin. The unicellular green alga Chlamydomonas mulating evidence that Pax 6 is the universal master control
has developed a visual system that allows it to measure light gene for eye morphogenesis in metazoa ranging from platy-
intensity, as well as to determine the direction of the incident helminths to humans. The universality of rhodopsin and Pax
light. These abilities confer a strong selective advantage for an 6 suggests that the different types of eye found in metazoa
organism that depends on photosynthesis35. The direction of are derived from a single prototypic eye and are, therefore,
the incident light is determined with the help of the eyespot, a of monophyletic origin. Pax 6 serves as a regulatory gene to
carotenoid-containing vesicle that presumably operates as an assemble the different cell-types, such as photoreceptor cells
interference reflector. The action spectra for phototaxis and and pigment cells, into a light-sensing organ. This new con-
flash-induced phobic responses have a maximum close to cept of eye evolution is illustrated in Fig. 1. Originating from
550 nm like rhodopsin, and in blind retinal-deficient cells, a precambrian prototype, the various types of eye are
positive phototaxis can be restored by supplying the cells with thought to have evolved by divergent, parallel and conver-
all-trans retinal. Chlamydorhodopsin has recently been gent evolution by recruiting numerous additional genes
cloned36, and it shows some sequence homology to inverte- into the eye-developmental pathways, as discussed in the
brate rhodopsins. However, it is not a typical seven-trans- following section.
membrane receptor, and looks instead rather like an ion In higher metazoa, the eyes are connected to the brain,
channel. Therefore, this primitive plant rhodopsin probably where visual information is processed and transmitted to the
diverged from animal opsin early in evolution. In all verte- effector organs, such as muscles. In the more primitive
(ancestral) cnidarians, such as cubomedusae (which do not
have a brain, but only a nerve ring around the umbrella), the
FIGURE 4. Retrograde and intercalary evolution eyes are directly connected to the muscles in the tentacles.
This suggests that the eye evolved as an information-gather-
(a)
ing organ before the brain, the information-processing
Histidine biosynthesis organ.

E1 E2 E7 E8 E9 Evolution of biosynthetic and morphogenetic

A B C W X Y Z pathways
Horowitz37 has proposed a mechanism for the evolution
ATP + PRPP (9 enzymes) Histidine
of biosynthetic (or biochemical) pathways that is based on
Evolution the idea of retrograde evolution (Fig. 4a). This hypothesis
(0) Histidine has to be taken up from the environment Z assumes that, for example, the nine enzymes in histidine
E9 biosynthesis evolved in a retrograde fashion. Presumably,
(1) Step Y Z primitive organisms had to take up histidine from the
E8 environment. The organisms that evolved the last enzyme
(2) Step X Y Z
in the pathway presumably had a strong selective advan-
E7
(3) Step W X Y Z
tage when the supply of histidine (Z) in the environment
was exhausted, because it could use compound Y and con-
(b) vert it to Z. The next step was the evolution of enzyme
and so on, until all nine enzymes had evolved that made it
Eye morphogenesis possible to achieve histidine biosynthesis from PRPP and
ATP. A similar mechanism of retrograde evolution has
X
C been proposed for the evolution of the sex-determination
Y
A B
pathway38.
Z Based on a similar kind of logic, we propose that
D morphogenetic (or developmental) pathways evolve by
Pax 6 Rhodopsin intercalary evolution (Fig. 4b). Prerequisite is the prior
evolution of rhodopsin and of Pax 6 to generate the proto-
Intercalation of genes trends in genetics
typic eye. The prototype, as pointed out by Darwin, cannot
be explained by selection, because selection can drive evo-
(a) Hypothetical retrograde evolution of histidine biosynthesis as proposed by Horowitz37. The last lution only when the eye can function at least to a small
enzyme (E9) of the biosynthetic pathway evolves first, followed by E8 in a second step. This proceeds extent. Once the prototype has evolved, presumably by sto-
until all nine enzymes are lined up in a linear pathway. (b) Proposed intercalary evolution of chastic events, selection can optimize it by a mechanism
morphogenetic pathways. First a rhodopsin-containing photosensitive cell has to evolve, that under
that can be called intercalary evolution to distinguish it
the control of Pax 6 is assembled with a pigment cell to form a functional eye prototype. The top of
the cascade is formed by a master control gene (Pax 6), the bottom by essential structural genes,
from retrograde evolution mentioned above. The proto-
such as rhodopsin. In the course of evolution, new genes are intercalated between the top and bottom type has acquired two key genes, Pax 6 on the top, and
of the cascade: regulatory genes, such as eyeless downstream of twin of eyeless; and structural rhodopsin at the bottom of the genetic cascade. In-
genes, such as the lens crystallin genes. The morphogenetic pathway is not linear but, rather, a creasingly complex and more-sensitive eyes can be gener-
complex network. ated by the intercalation of genes into the cascade (Fig. 4b).
At least three genetic mechanisms for intercalation are
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Eye morphogenesis and evolution Perspectives

known. First, gene duplication and divergence, as de- has been termed gene sharing or recruitment. Third, the
scribed for ey and toy. The original autocatalytic feedback recombination of various coding and regulatory regions of
loop is converted to a heterocatalytic loop, where toy different genes by‘evolutionary tinkering’ might also lead
regulates ey, the latter becoming intercalated into the eye to recruitment and intercalation into a new morphogenetic
morphogenetic path-way downstream of toy16. Second, pathway.
recruitment of novel genes into the morphogenetic path- These considerations clearly have a bearing on our
way by fusion of the coding region of a gene to an eye- concepts of homology. Homology is not an all-or-
specific enhancer or promoter. Piatigorsky39 has described nothing phenomenon, because two different types of
several examples of this kind. Genes encoding enzymes like eye might only be partially homologous and they can also
enolase or lactate dehydrogenase, or small heat shock pro- have acquired analogous features as proposed by
teins are recruited into the eye morphogenetic pathway as Zuckerkandl40. This will resolve discrepancies in the inter-
lens proteins called crystallins. This evolutionary process pretation41 of these new findings in eye evolution.

References 16 Czerny, T. et al. (1999) Twin of eyeless, a second Pax 6 gene of a complex and function synergistically to induce ectopic eye
1 Salvini-Plawen, L. and Mayr, E. (1961) in Evolutionary Biology, Drosophila, acts upstream of eyeless in the control of eye development in Drosophila. Cell 91, 893–903
(Vol. 10) (Hecht, M.K., Steere, W.C. and Wallace, B., eds), development. Molecular Cell 3, 297–307 29 Pan, D. and Rubin, G.M. (1998) Targeted expression of teashirt
pp. 207–263, Plenum Press 17 Cadigan, K.M. et al. (1994) Functional redundancy: the respective induces ectopic eyes in Drosophila. Proc. Natl. Acad. Sci. U. S. A.
2 Lewis, E.B. (1992) Clusters of master control genes regulate the roles of the two sloppy paired genes in Drosophila segmentation. 95, 15508–15512
development of higher organisms. J. Am. Med. Assoc. 267, Proc. Natl. Acad. Sci. U. S. A. 91, 6324–6328 30 Jang, C-C. et al. Two Pax genes, eye gone and eyeless, act in parallel
1524–1531 18 Halder, G. et al. (1998) Eyeless initiates the expression of both in determining Drosophila eye development. Development (in press)
3 Schneuwly, S. et al. (1987) Redesigning the body plan of sine oculis and eyes absent during Drosophila compound eye 31 Toy, J. et al. (1998) The Optx2 homeobox gene is expressed in
Drosophila by ectopic expression of the homeotic gene development. Development 125, 2181–2191 early precursors of the eye and activates retina specific genes.
Antennapedia. Nature 325, 816–818 19 Plaza, S. et al. (1993) Quail Pax 6 (Pax-QNR) encodes a Proc. Natl. Acad. Sci. U. S. A. 95, 10643–10648
4 Walther, C. and Gruss, P. (1991) Pax 6, a murine paired box gene, transcription factor able to bind and trans-activate its own 32 Mathers, P.H. et al. (1997) The Rx homeobox gene is essential for
is expressed in the developing CNS. Development 113, 1435–1449 promoter. Cell Growth Differ. 4, 1041–1050 vertebrate eye development. Nature 387, 603–607
5 Hill, R.E. et al. (1991) Mouse Small eye results from mutations in 20 Niimi, T. et al. Direct regulatory interaction of the eyeless protein 33 Eggert, T. et al. (1998) Isolation of a Drosophila homolog of the
a paired-like homeobox-containing gene. Nature 354, 522–525 with an eye-specific enhancer in the sine oculis gene during eye vertebrate homeobox gene Rx and its possible role in brain and
6 Ton, C.C.T. et al. (1991) Positional cloning and characterization induction in Drosophila. Dev. Biol. (in press) eye development. Proc. Natl. Acad. Sci. U. S. A. 95, 2343–2348
of a paired box- and homeobox-containing gene from the Aniridia 21 Cheyette, B.N.R. et al. (1994) The Drosophila sine oculis locus 34 Khorana, H.G. (1992) Rhodopsin, photoreceptor of the rod cell.
region. Cell 67, 1059–1074 encodes a homeodomain-containing protein required for the J. Biol. Chem. 267, 1–4
7 Jacob, F. (1997) Evolution and tinkering. Science 196, 1161–1166 development of the entire visual system. Neuron 12, 977–996 35 Foster, K.W. et al. (1984) A rhodopsin is the functional
8 Quiring, R. et al. (1994) Homology of the eyeless gene of 22 Serikaku, M.A. and O’Tousa, J.E. (1994) sine oculis is a homeobox photoreceptor for phototaxis in the unicellular eukaryote
Drosophila to the Small eye gene in mice and Aniridia in humans. gene required for Drosophila visual system development. Chlamydomonas. Nature 311, 756–759
Science 265, 785–789 Genetics 138, 1137–1150 36 Deininger, W. et al. (1995) Chlamyrhodopsin represents a new
9 Hoge, M.A. (1915) Another gene in the fourth chromosome of 23 Bonini, N.M. et al. (1993) The eyes absent gene: genetic control of type of sensory photoreceptor. EMBO J. 14, 5849–5858
Drosophila. Am. Nat. 49, 47–49 cell survival and differentiation in the developing Drosophila eye. 37 Horowitz, N.H. (1945) On the evolution of biochemical syntheses.
10 Halder, G. et al. (1995) Induction of ectopic eyes by targeted Cell 72, 379–395 Proc. Natl. Acad. Sci. U. S. A. 31, 153–157
expression of the eyeless gene in Drosophila. Science 267, 24 Bonini, N.M. et al. (1997) The Drosophila eyes absent gene directs 38 Wilkins, A.S. (1995) Moving up the hierarchy: a hypothesis on the
1788–1792 ectopic eye formation in a pathway conserved between flies and evolution of a genetic sex determination mechanism. BioEssays
11 Altmann, C.R. et al. (1997) Lens induction by Pax 6 in Xenopus vertebrates. Development 124, 4819–4826 17, 71–11
laevis. Dev. Biol. 185, 119–123 25 Mardon, G. et al. (1994) dachshund encodes a nuclear protein 39 Piatigorsky, J. and Wistow, G.J. (1989) Enzyme/crystallins: gene
12 Hauck, B. et al. Functional analysis of an eye specific enhancer of the required for normal eye and leg development in Drosophila. sharing as an evolutionary strategy. Cell 57, 197–199
eyeless gene in Drosophila. Proc. Natl. Acad. Sci. U. S. A. (in press) Development 120, 3473–3486 40 Zuckerkandl, E. (1994) Molecular pathways to parallel evolution:
13 Xu, P-X. et al. (1999) Regulation of Pax 6 expression is conserved 26 Shen, W. and Mardon, G. (1997) Ectopic eye development in I. Gene nexuses and their morphological correlates. J. Mol. Evol.
between mice and flies. Development 126, 383–395 Drosophila induced by directed dachshund expression. 39, 661–678
14 Loosli, F. et al. (1996) Isolation of a Pax 6 homolog from the Development 124, 45–52 41 Abouheif, E. et al. (1997) Homology and developmental genes.
ribbon worm Lineus sanguineus. Proc. Natl. Acad. Sci. U. S. A. 93, 27 Pignoni, F. et al. (1997) The eye-specification proteins So and Eya Trends Genet. 13, 432–433
2658–2663 form a complex and regulate multiple steps in Drosophila eye 42 Jacobs, D.K. et al. (1998) in Molecular Approaches to Ecology and
15 Tarpin, M. et al. Reverse homeosis in homeotically reconstructed development. Cell 91, 881–891 Evolution (De Salle, R. and Schierwater, B., eds), pp. 323–357,
ribbonworms. Nature (in press) 28 Chen, R. et al. (1997) Dachshund and Eyes Absent proteins form Birkhäuser

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 PERSPECTIVES
can guide us in a similar understanding of
OPINION
homology among morphological structures.
Two genes are homologous as long as they
The developmental genetics are derived from the same gene in a com-
mon ancestor, regardless of whether they
of homology have the same function and regardless of
the extent of similarity in their nucleotide
sequences. The gene retains its identity
Günter P. Wagner despite evolutionary change in its function
and sequence, as long as all changes result
Abstract | Homology is an essential idea of biology, referring to the historical from mutations at the same genomic locus.
continuity of characters, but it is also conceptually highly elusive. The main The basis of gene identity is the historical
difficulty is the apparently loose relationship between morphological continuity of the locus undergoing evolu-
characters and their genetic basis. Here I propose that it is the historical tionary change. Of course, things become
continuity of gene regulatory networks rather than the expression of individual more complicated with gene duplications
and loss or fusion of parts of genes (for
homologous genes that underlies the homology of morphological characters.
example, exon shuffling) to form new genes,
These networks, here referred to as ‘character identity networks’, enable the and when extensive sequence divergence
execution of a character-specific developmental programme. erases the evidence of shared ancestry. The
mode of evolution that preserves the histori-
Characters found in different species are can be variable. These networks control the cal identity of a gene is the replacement of
homologous if they are derived from the execution of character-specific developmental alleles at the same genomic locus.
same character in their most recent common programmes, which allow for quasi-
ancestor (MRCA), regardless of similarity independent variation of characters5 with Homology of morphological characters:
in form or function (FIG. 1). Whenever we respect to other parts of the body. what does ‘sameness’ mean? The homol-
compare two or more species, or use a model ogy of morphological characters is also a
organism to learn about the molecular What does homology mean? case of historical continuity in the face of
basis of human disease, we implicitly need In the eighteenth and nineteenth centuries, it descent with modification. In a population,
to identify corresponding body parts and became clear that the similarities and differ- a character exists in different states of size,
functional systems; that is, we make assess- ences among organisms are not random, but shape or colour. Evolutionary change usu-
ments about homology. Intuitively, one follow patterns that call for an explanation. ally proceeds by changing the frequency
would expect that the historical continuity of Most intriguing are the similarities among of these character states in the population,
morphological characters is underpinned by some body parts that cannot be explained by eventually leading to the replacement of
the continuity of the genes that govern the shared functional necessity. For example, the the ancestral character state by a derived
development of these characters. However, tetrapod limb shows a highly stereotypical character state (FIG. 1). Sameness, then, by
things are not that simple: one of the most pattern of bony elements (FIG. 2), regardless the definition of homology, does not refer to
important results of the past 15 years of of whether it is used for running, flying, similarity of structure or function as such,
molecular developmental genetics is the swimming or grasping. This pattern was but to historical continuity through inherit-
realization that homologous characters can conceptualized by Richard Owen as homol- ance with modification. In other words,
have different genetic and developmental ogy 6, paving the way for the theory of the homology concept can be applied to
bases1–3. This seems paradoxical, because evolutionary change. Even today, the exist- anything that forms a lineage10–13. Of
the historical continuity of morphological ence of homologous body parts in different course, things become more complicated
characters implies continuity of the (genetic) animals and plants is cited as standard when new characters arise (novelties) or
information about the characters4. But where evidence for this process7. characters duplicate like genes (for example,
else should we look for this continuity, other teeth or fins).
than in the genes? Here I review some of The easy case: homology of genes. Since At the formal phenomenological level,
the conceptual issues, and the experimen- the time of Owen and Darwin, the idea of a morphological character corresponds to a
tal results that suggest a solution to this homology has been extended to other bio- genomic locus, and a character state to an
conundrum. I argue that the continuity of logical entities, such as genes, nucleotides, allele14 (BOX 1). Hence, in a more technical
morphological characters could be under- physiological processes and behavioural sense, a character is a unit of evolutionary
written by homologous regulatory networks patterns7,8. What it means to speak of change at the phenotypic or morphological
of co-adapted transcription factor genes, homologous genes is well understood9, and level in the same way that a gene is the unit
whereas other aspects of their development I recapitulate these ideas here because they of evolutionary change at the genetic level15.

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Developmental genetics and homology? other animals that is not segmented and, segment formation2. Surprisingly, the most
The semi-conservative mode by which furthermore, the insects are nested in an extensive interspecific variation has been
DNA replicates ensures that genes directly even larger clade, the arthropods, which found in the higher levels of the segment-
give rise to copies of themselves, and consists exclusively of segmented animals. ation hierarchy, namely the gap genes and
is therefore the mechanistic basis for Yet some genes that are essential for the pair-rule genes2,23. Examples are the
their historical continuity. In the case of segmentation in Drosophila melanogaster20, pair-rule genes ftz and eve, mentioned above,
morphological characters, however, the for example, the pair-rule genes fushi and the gap gene bicoid (bcd), which exists
situation is more complicated, because tarazu (ftz) and even skipped (eve), do not only in the higher Diptera, not even in the
morphological characters and even cell have pair-rule function in the grasshopper dipteran mosquito Anopheles. By contrast,
types do not usually directly spawn copies Schistocerca americana, but are instead the segment-polarity gene network, which
of themselves between generations, but expressed in the developing CNS21,22. includes the interaction of engrailed (en)
are recreated in each generation from a Clearly, the way in which segments are and wingless (wg), seems to be invariant, at
single cell, the zygote16. The recreation of formed in development has changed since least among insects2. This suggests that the
a character is controlled by developmental the MRCA of crown-group insects. genetic regulatory network (GRN) that con-
genes, so it is tempting to speculate that A solution to this conundrum can be trols the execution of the segment-specific
the continuity of morphological characters found in the fact that developmental morphogenetic processes is less variable
can be explained by the continuity of variation in homologous characters is not than the upstream processes that activate it.
genetic information. Since the beginning randomly distributed, but affects some If the pattern that is suggested by the data
of experimental developmental biology in aspects of development more than others. on insect segmentation can be generalized, it
the early twentieth century, the emerging For example, in D. melanogaster, segmenta- seems that the most conservative parts
picture has been disappointing and tion proceeds through three stages that are of the developmental process are the
confusing2,17–19. For instance, there is no controlled by particular genes: gap genes, GRNs that control the developmental
question that body segments in all orders which determine larger body regions, the programme that specifies the identity of
of insects are homologous and derived pair-rule genes, which divide the embryo the character; that is, the character identity
from a single common ancestor — there into stripes of alternating half segments, network (ChIN). For example, individual
is not a single lineage of organisms more and the segment-polarity genes, which cell types are determined by a characteristic
closely related to an insect group than to activate the actual morphogenetic process of set of regulatory genes over vast evolutionary
distances24–27. Another example is the genetic
network for the endomesoderm that starfish
and sea urchins share28. By contrast, other
aspects of development, from early pattern-
ing to the execution of the developmental
a programme, are more variable2.
Here I review evidence that shows
that these networks determine character
identity rather than character state, that
non-homologous morphological characters
are determined by non-homologous ChINs,
and that the genes participating in a ChIN
are co-adapted for their task; that is, they are
functionally non-equivalent to orthologues in
species that do not have the character, and
to paralogues that do not participate in the
development of that character.
c
b
ChIN genes determine character identity
The idea that the genes that control character
identity are distinct from the genes that
determine the special shape and state of
a character has been well documented in
the case of Ultrabithorax (Ubx) function
in insect wing development. Ancestrally,
pterygote (or winged) insects have two
pairs of proper wings associated with T2
and T3 (the second and third segments in
Figure 1 | Homology of morphological characters. The hand of a human (part a) differs greatly in
terms of detailed structure and function from the wing of a bird (part b), but both are considered
the thorax), as seen, for instance, in honey
homologous because they arose from a corresponding character in the tetrapod common bees, grasshoppers and most spectacularly
ancestor(part c) through descent with modification. This figure illustrates that morphological in butterflies (FIG. 3a). Dipterans have only
characters form lineages of descent in the same way that genes form unique lineages of descent, one pair of wings, which is localized on T2;
as long as they are not duplicated. Homology is the historical continuity of characters in multiple that is, they are forewings. A homologue of
lineages despite variations in their character state. the hind wing lies on T3 but does not take

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Whale Frog Horse Lion Human Bat Bird

Figure 2 | Homologous characters can have different shapes and func- explain the similarity of the basic construction of homologous characters.
tions. Forelimbs of seven tetrapod species exemplify the fact that This remains one of the standard arguments in favour of evolution; that
corresponding body parts have a similar design but can serve different is, that species derive from common ancestors by a process of descent
functions, from swimming to flying. Hence, functional necessity cannot with modification.

the shape of a wing blade. Instead, it is a Experimental evidence shows that this ChINs of non-homologous characters
small, club-like appendage called the haltere distinction between character identities The GRN underlying eye development
(FIG. 3b). Beetles also have only one pair of and character states is the result of different is a celebrated example of evolutionary
wing blades, but as they are associated with genetic underpinnings. ChIN genes, like conservation, as it suggests that there is
T3 they are hind wings. The forewings in Ubx and abdominal-A (abdA), determine homology between vertebrate and insect
beetles have been transformed into a pair of character identity (forewing versus hind eyes34. This assertion largely comes from the
highly scleratized structures, called elytra, wing) across species, regardless of their common role of paired-box gene 6 (Pax6) in
that function as protective covers (FIG. 3c). So, character state30. In D. melanogaster, a the two systems, but detailed studies show
butterflies, flies and beetles all have two pairs loss-of-function mutation of Ubx leads to that the rest of the network is strikingly
of dorsal appendages that are homologous, the development of a second set of wing different (see below). The most parsimoni-
because they are nested within a larger blades (FIG. 4a). This does not mean that Ubx ous interpretation is that Pax6 is part of
clade of winged insects, almost all of which function is to suppress wing development; the ancestral cell-differentiation pathway
have two pairs of wings on their T2 and T3: Warren and collaborators demonstrated for photoreceptors and was then separately
the forewings, which are flying organs in that the four-winged butterfly also expresses incorporated into the ChINs for both types
flies and butterflies but protective organs Ubx in its T3 (REF. 31). So, in general Ubx of image-forming eyes28.
in beetles, and the hind wings, which form determines hind wing identity, regardless of
functional wing blades in butterflies and whether the hind wing is shaped as a wing
beetles but are sensory organs (halteres) in blade or a haltere, as in dipterans32. This
dipteran insects. was confirmed in the flour beetle Tribolium Glossary
Hence, morphologically, we can distin- castaneum33. As in the butterfly, the beetle Orthologue
guish between two kinds of entities. On the expresses Ubx in T3, and suppression of Two genes are orthologues if their lineages are connected
through a speciation event and without a duplication event.
one hand, there are two character identities: Ubx function by RNAi leads to a second
forewings and hind wings. On the other set of elytra on T3 (FIG 4b). Clearly, Ubx Paralogue
hand, there are various character states does not determine the shape of a wing but Two genes are paralogues if their lineages are connected
that insect wings can assume: the forewing determines hind-wing identity “…regardless through a gene duplication event.
can be a wing blade or an elytra, and the of form and function” 6,30. The character
Pro-orthologue
hind wing can be a wing blade or a haltere. state can change in evolution, but it remains For example, when one species has two copies of a gene,
Distinguishing between character identi- under the control of Ubx. say Ga and Gb, and another species has a single copy G,
ties and character states also removes the The experimental evidence that is cited and the speciation event that separated the species
confusion that is inherent in the character here pertains to only one gene, Ubx, but lineages occurred earlier than the gene duplication event,
G is the pro-orthologue of Ga and Gb.
concept29 between parts, such as wings and it is unlikely that Ubx is acting alone. One
legs (character identities), and attributes would expect that Ubx is part of a small Semi-orthologue
of parts, such as size, shape and colour network that also includes abdA and other For example, if G is the pro-orthologue of Ga and Gb, then
(character states). transcription factor genes. both Ga and Gb are the semi-orthologues of G.

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Box 1 | Equivalent terms for genes and morphological characters do not regulate Dach1, the homologue of
D. melanogaster dac.
Morphological characters are equivalent to a genetic locus that undergoes evolutionary There are two possible reasons for the
modification. Different instantiations of a gene are called alleles and different instantiations of a dissimilarity between the GRNs of eye develop-
character are called character states. Genes that were inherited from a common ancestor without
ment in D. melanogaster and vertebrates. It
duplication are orthologues, whereas body parts in two species that were inherited from a common
ancestor are homologues. Different instances of a gene caused by gene duplication are called
could be that the MRCA of flies and mam-
paralogues, and repeated instances of a morphological character in the same organisms are mals had a GRN that involved members from
called serial homologues. New genes can arise through gene duplication and divergence or from the all four gene families, but this network later
fusion of parts of genes. For morphological characters, a new character that creates a new lineage of changed. Alternatively, it could be that, just
descent with modifications is called an evolutionary novelty67. These can arise in various ways, for as the image-forming eye structures are inde-
instance, by duplication and differentiation, much like for new genes, or by de novo origination. pendently derived, the regulatory interactions
Genetic terms and their equivalents for morphological characters: among these genes in eye development also
evolved independently, and the GRN was not
Genetic term Morphological equivalent present in the MRCA of flies and mammals.
Locus Character The gene lineages of the Six gene family
Allele Character state suggest that the latter is the case. Although
Six and Pax genes tend to be expressed
Orthology Special homology
together in various organs and cell types41,42,
Paralogy Serial homology the different Six genes that are involved in
Origin of new genes Evolutionary novelty D. melanogaster and vertebrate eye develop-
ment are not orthologues. According to
a phylogenetic analysis of Six genes from
animals and unicellular flagellates, so of
In D. melanogaster, the gene eyeless All the genes in the D. melanogaster eye D. melanogaster and optix from vertebrates
(ey; with homology to the Pax gene ChIN are members of larger gene families are ancient paralogues predating the origin
family in vertebrates) is necessary for eye (TABLE 1). In vertebrates, genes from these of multicellular animals44,45. Hence, it is most
development and is sufficient to induce four gene families (Pax, Six, Eya and Dach) parsimonious to assume that so and the
eyes35. In fact, ey is part of a small are also involved in the development of optix genes were independently recruited
network that includes another transcrip- several other organs and tissues, such as into eye development in the vertebrate and
tion factor, sine oculis (so; with homology muscle and ear41,42. insect lineages just as their morphological
to the Six gene family in vertebrates) and However, the GRN of eye morphogen- eye structures are independently derived.
two transcriptional cofactors, eyes absent esis in vertebrates is not the same as that in This shows that ChINs differentiate as they
(eya) and dachshund (dac), and is activated D. melanogaster37,41,43 (FIG. 5). For instance, assume control of the development of a new
by a paralogue of ey called twin of eyeless Pax6/ey is upregulated by non-homologous character, so that different characters are
(toy) (FIG. 5a). Surprisingly, it was found genes in the two systems43: in insects, ey is controlled by non-orthologous sets of genes.
that homologous genes, most notably regulated by toy, whereas in vertebrates, Furthermore, the ciliary, vertebrate-type
Pax6, which is the pro-orthologue36 of ey, the transcription factor gene retinal home- photoreceptor and the rhabdomeric, insect-
are involved in eye development in all obox (Rx; also known as Rax) is upstream type photoreceptor coexist in a polychaete
animals that have been examined34,37–39, of Pax6. Although a D. melanogaster worm, Platynereis dumerilii, showing that
and can induce ectopic eyes in homologue of Rx does exist, it is not vertebrate and insect eyes derive from ‘paral-
D. melanogaster35 as well as in Xenopus involved in eye development. Similarly, in ogous’ cell populations25,46 and are therefore
laevis40. vertebrates, Eya1,2,3 (homologues of eya) likely to be non-homologous.

a b c

Figure 3 | Characters and character states. The insects shown all have two is the forewing, whereas the hind wing is transformed into a club-shaped
pairs of dorsal appendages, forewings and hind wings. They can both be wing appendage, termed the haltere (indicated by a black arrow). In beetles, the
blades that function in producing lift, as in the case of butterflies (panel a), proper wing blade is the hind wing, whereas the forewing is transformed
or only one might form a proper wing blade, as in Diptera (panel b) or beetles into a protective cover called the elytra (indicated by a white arrow). Images
(panel c). In the Diptera (flies, mosquitos and so on), the proper wing blade in panels b,c courtesy of J. Tanis and A. Andrasi, respectively.

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a b of the protein, with a QAQAQK(A)n motif

(QA motif)53. Similar results were obtained
in a comparison of D-UBX1A and
A. franciscana Ubx (Af-Ubx) by McGinnis
and collaborators55. In another study in
D. melanogaster, in which the wild-type
Ubx allele was replaced with an allele in
which the QA motif was deleted (UbxΔQA)54,
it was shown that QA has an additive effect
together with other peptide motifs60 and
ABDA protein activity. This series of stud-
Figure 4 | Ubx determines character identity, not character states. Loss of Ultrabithorax (Ubx) func- ies shows that functional non-equivalence
tion leads to development of a forewing in the position of the hind wing (in body segment T3), regardless of UBX evolved not through changes in the
of the character state. In Drosophila melanogaster (panel a), a loss-of-function mutation of Ubx leads DNA binding activity of the transcription
to two forewings, whereas in Tribolium castaneum (panel b) the knockdown of Ubx leads to a second set factor, but most likely through changes
of elytra33. So, Ubx is necessary to determine hind wing identity but does not determine character
in protein–protein or protein–RNA
state30. Part b reproduced with permission from Nature REF. 33 © (2005) Macmillan Publishers Ltd.
interactions.
Two important studies show that there
are also specific functional differences
Unfortunately, little is known about the equivalent in evolution, and that these between the homeodomains of Hox genes
genetics of cephalopod eyes47,48, the third differences are not due to changes in DNA within the same organism (the mouse in
type of independently derived complex binding, but rather to changes in protein– this case). Zhao and Potter58,59 replaced
light-sensory organs. If the ChIN concept protein interactions among transcription the HoxA11 homeobox with the HoxA13
is correct, one would predict that the GRN factors. homeobox (creating HoxA11(a13Hd)) and
of cephalopod eye development includes A particularly well investigated found that this allele can rescue the
Pax6 but is otherwise independently case of functional non-equivalence is HoxA11–/– phenotype in the development of
derived, and different from both the insect that of Ubx in D. melanogaster compared the body axis, kidney and male reproduc-
and the vertebrate eye GRN. with its homologues in the velvet worm tive tract. Interestingly, the HoxA11(a13Hd)
Acanthokara kaputensis52,53 and the brine allele antagonizes normal HoxA11 function
Co-adapted transcription factors shrimp Artemia franciscana55. Grenier in limb development and causes homeotic
What mechanism keeps the GRNs that and Carroll52 compared the in vivo activ- transformation of the uterine epithelium
determine character identity more con- ity of A. kaputensis Ubx (Onychophora: into cervical epithelium.
served than other aspects of development? O-Ubx) with that of D. melanogaster This study was followed up with homeo-
A possible answer to this question derives Ubx1a (D-Ubx1a) in a misexpression domain swapping experiments between
from the fact that transcription factor approach. O-Ubx and D-UBX1A have HoxA11, HoxA10 and HoxA4 (REF. 59).
proteins do not remain equivalent, but similar homeodomains (97% identical HoxA10 is even more similar to HoxA11
undergo functionally important changes amino-acid sequence), but their overall than HoxA13, and the HoxA11(a10Hd) allele
during evolution, particularly with respect similarity is low. O-UBX is only 214 amino was functionally quasi-equivalent even in
to protein–protein interactions. This is acids long, compared with 380 amino acids the female reproductive tract, in addition
a well documented but often overlooked in D-UBX1A. Like D-UBX1A, O-Ubx to the body axis, kidney and male repro-
fact of the evolution of gene regulation. It expressed in flies can transform antenna ductive tract. By contrast, replacing the
is now well established that the functional towards a leg phenotype and forewings HoxA11 homeodomain with that of HoxA4
specificity of transcription factors is not into halteres. More specifically, O-Ubx can led to near-recessive null function in all
solely related to DNA binding specificity, repress Surf wings (Srf) in the wing disc but the axial development.
which is low, but also involves interactions and drive the expression of decapentaplegic The pattern emerging from these stud-
with other transcription factor proteins49, (dpp) in the visceral mesoderm, both of ies is that functional non-equivalence is
and differences in the functional activity of which are specific targets of D-UBX1A. more likely for more derived functions,
a transcription factor depend on parts But other typical effects of D-Ubx cannot such as the mammalian female reproduc-
of the protein that are not engaged in DNA be reproduced by O-Ubx, such as tive tract, than for more ancient characters,
binding. These functionally important repression of Distal-less (Dll) in the leg such as body axis. That is, the older the
differences in transcription factor proteins rudiments. These D-UBX1A-specific activ- paralogues and the more derived
might lead to co-adaptation among the ities are caused by differences outside the the characters, the less likely it is that the
transcription factor genes that partake in homeodomain. The authors suggest that transcription factors are still functionally
the same GRNs. Although several lines D-UBX1A can engage in protein–protein equivalent. These results are interesting
of evidence have created the misleading interactions specific for these characters in light of the recent findings of adaptive
impression that transcription factors are that O-Ubx cannot, although the specific evolution of the homeodomain following
functionally invariant50, there is a growing interaction partners have not been identi- Hox gene duplication61, and the fact that
amount of compelling evidence51 that fly fied. In a later paper, the sequence that paralogue-specific amino-acid residues in
transcription factor genes like Ubx52–55, is responsible for the D-UBX1A-specific the homeodomain are likely to function
tinman (tin)56, and ftz57, as well as vertebrate activity was identified as a repressor in protein–protein interactions rather than
Hox genes58,59, do not remain functionally domain on the carboxy (C)-terminal side DNA binding62.

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Drosophila melanogaster Xenopus laevis Certainly, Hox-gene-based GRNs are likely

toy Optx2 Six 3 Lhx2 candidates for ChINs, but are not kernels
according to Davidson’s use of the term28.
Any new character is expected to have its
ChIN, regardless of how old it is, whereas
(Rx) ey so
kernels are supposed to be associated with
ET Rx Pax6 Tll and be invariant in the oldest clades in the
animal kingdom. Kernels and ChINs are
both classes of GRN, but they serve differ-
ent conceptual ends and are only partially
dac eya ( Dach1 ) Eya1,2,3
overlapping.
Figure 5 | Gene regulatory networks for eye development. The non-homologous eyes of insects
and vertebrates are controlled by non-homologous genetic regulatory networks37,39. In Drosophila Future directions
melanogaster, the five genes eyeless (ey), twin of eyeless (toy), eyes absent (eya), dachshund (dac) and Consistent with modern views of homo-
sine oculis (so) are jointly necessary for eye development. Four of these are also sufficient to induce logy10,11,13,65,66, character identity is not tied
eye development and can mutually induce each other’s expression: toy, ey, eya and dac. The retinal to particular manifest features, like struc-
homeobox (Rx) transcription factor gene, which is essential in vertebrate eye development, is also ture, composition and shape. Instead,
present in the D. melanogaster genome but is not involved in eye development. dac is essential in homologues have a single historical origin,
D. melanogaster eye development, but its semi-orthologue, Dach1, is not essential in vertebrate (for form a lineage of descent with modification,
example, Xenopus laevis) eye development. For vertebrates, similar genes are involved in eye devel-
and can go extinct. From a developmental
opment but the functional relationships among them are different and involve non-orthologous
genes. Orthologous genes are in red boxes and paralogous genes are in blue boxes. Instead of the point of view, character identity and thus
vertebrate semi-orthologue of sine oculis, the genes sine oculis homeobox homologue 3 (Six3) and homology requires the ability to express
Optx2 (also known as Six6) are involved in eye development. The gene duplication event that an evolutionarily variable developmental
created the sine oculis and the Six3/Optx2 paralogues occurred long before the most recent com- programme that is different from those
mon ancestor of insects and vertebrates44,45. This shows that the genetic regulatory networks of in other parts of the body. In this paper, I
insect and vertebrate eye development are most likely not homologous but derived independently. propose that this capability is underwritten
ET, transcription repression factor Tbx3; Lhx2, LIM homeobox 2; Pax6, paired-box 6; Tll, nuclear by GRNs of co-adapted transcription factor
receptor subfamily 2, group E, member 1, nr2e1-A, Xtll. genes. This concept implies a number of
predictions that can be tested with the aid
of standard gene knockdown and rescue
The few examples reviewed above show and which are dedicated to a specific experiments and functional genomic tools.
that a transcription factor that becomes developmental function.”28 Although For instance, the knockdown of a transcrip-
involved in a novel character has a tendency instances of kernels certainly overlap with tion factor gene that is part of a ChIN
to become modified to carry out that novel examples of ChINs, the conceptual goal should affect the majority of genes that are
function. This probably happens because of differs. From Davidson’s examples, it is regulated during the development of that
co-adaptation among transcription factors clear that kernels are only the most con- character. In addition, because the members
in the same GRN63, but because there is no served GRNs regardless of their biological of a ChIN are assumed to be jointly neces-
published example in which the evolution function. For instance, Hox GRNs do not sary for the development of the character,
of both protein–protein interaction partners constitute kernels because they are not old the knockdown of different members is
has been documented, we cannot be sure or invariant enough. By contrast, ChINs are predicted to affect largely overlapping
that this is the case. It could be that we see defined as GRNs that subscribe the execu- sets of downstream genes. The assertion
the result of adaptation of one transcription tion of a character-specific developmental that members of a ChIN are co-adapted
factor to another without both of them programme, regardless of how old they are. can be tested by rescue experiments.
evolving. In either case, the transcription
factors in a ChIN for a specific character
are specialized for this task and remain Table 1 | Gene families in eye development: the Pax, Ey, Six, Eya and Dach families
associated with each other and with their Cnidarians Drosophila melanogaster Vertebrates
character. They thus share historical PaxA Pox neuro
continuity with the character they control.
PaxB sparkling (also known as shaven) Pax2, Pax5, Pax8
ChINs and other GRNs. In a recent syn- PaxC eyeless, twin of eyeless Pax4, Pax6
thesis of the current knowledge of GRN PaxD Pox meso, gooseberry, gooseberry neuro, paired Pax3, Pax7
evolution, Eric Davidson also noted that Six1/2 sine oculis Six1, Six2
interspecific variation in GRNs is non-
random64. He coined the term ‘kernel’ for Six3/6 Optix Six3, Optx2
the most conserved set of GRNs28, and Six4/5 myotonix Six4, Six5
it is legitimate to ask whether the kernel ? eyes absent Eya1, Eya2, Eya3, Eya4
concept is equivalent to the ChIN concept
? dachshund Dach1, Dach2
proposed here. Davidson defines a kernel
See REFS 41,45,68,69. Note that the sine oculis and Optix genes duplicated before the most recent common
as “…[a] conserved subcircuit consisting ancestor of cnidarians and the bilaterian animals. ? indicates that family members have not been identified so far.
of genes which interact with one another Dach, dachschund family; Ey, eyeless family; Eya, eyes absent family; Pax, paired-box family; Six, sine oculis family.

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Ann. Rev. Ecol. Syst. 20, 51–69 (1989). Dev. Genes Evol. 214, 342–351 (2004). Acknowledgements
17. Hall, B. K. in Evolutionary Biology Vol. 28 45. Stierwald, M., Yanze, N., Bamert, R. P., The author gratefully acknowledges the financial support for
(eds Hecht, M. K., MacIntyre, R. J. & Clegg, M. T.) Kammermeier, L. & Schmid, V. The sine oculis/Six class the research that led to the ideas expressed in this article:
1–30 (Plenum, New York, 1994). family of homeobox genes in jellyfish with and without NSF IBN#0321470, OIB#0445971 and the Research Prize
18. Wray, G. A. & Abouheif, E. When is homology not eyes: development and regeneration. Dev. Biol. 274, from the Alexander von Humboldt Foundation. I also want to
homology? Curr. Opin. Genet. Dev. 8, 675–680 (1998). 70–81 (2004). thank the reviewers of this paper as well as M. Laubichler,
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underlying homology and homoplasy as seen through Dorresteijn, A. W. & Wittbrodt, J. Cilliary members of my laboratory for discussion and inspiration.
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The following terms in this article are linked online to:
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abdA | bcd | dac | Dach1 | dpp | en | eve | ey | eya | ftz | HoxA4 |
Dax, a locust Hox gene related to fushi-tarazu but Mann, R. S. The DNA binding specificity of
HoxA10 | HoxA11 | HoxA13 | Pax6 | Rx | so | Srf | tin | toy |
showing no pair-rule expression. Development 120, Ultrabithorax is modulated by cooperative
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23. Peel, A. D., Chipman, A. D. & Akam, M. Arthropod Cell 78, 603–615 (1994). FURTHER INFORMATION
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 JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 285:19–26 (1999)

Why Do Almost All Mammals Have Seven Cervical

Vertebrae? Developmental Constraints, Hox Genes,
and Cancer
FRIETSON GALIS*
Institute for Evolutionary and Ecological Sciences, University of Leiden,
2300RA Leiden, The Netherlands

ABSTRACT Mammals have seven cervical vertebrae, a number that remains remarkably con-
stant. I propose that the lack of variation is caused by developmental constraints: to wit, changes
in Hox gene expression, which lead to changes in the number of cervical vertebrae, are associated
with neural problems and with an increased susceptibility to early childhood cancer and still-
births. In vertebrates, Hox genes are involved in the development of the skeletal axis and the
nervous system, among other things. In humans and mice, Hox genes have been shown also to be
involved in the normal and abnormal (cancer) proliferation of cell lines; several types of cancer in
young children are associated with abnormalities in Hox gene expression and congenital anoma-
lies. In these embryonal cancers the incidence of a cervical rib (a rib on the seventh cervical
vertebra, a homeotic transformation of a cervical vertebra towards a thoracic-type vertebra) ap-
pears to be increased. The minimal estimate of the selection coefficient acting against these muta-
tions is about 12%.
In birds and reptiles variations in the number of cervical vertebrae have frequently occurred
and there is often intraspecific variability. A review of the veterinary literature shows that cancer
rates appear lower in birds and reptiles than in mammals. The low susceptibility to cancer in
these classes probably prevents the deleterious pleiotropic effect of neonatal cancer when changes
in cervical vertebral number occur.
In mammals there is, thus, a coupling between the development of the axial skeleton and other
functions (including the proliferations of cell lines). The coupling of functions is either a conserved
trait that is also present in reptiles and birds, but without apparent deleterious effects, or the
coupling is new to mammals due to a change in the functioning of Hox genes. The cost of the
coupling of functions in mammals appears to be an increased risk for neural problems, neonatal
cancer, stillbirths, and a constraint on the variability of cervical vertebral number. J. Exp. Zool.
(Mol. Dev. Evol.) 285:19–26, 1999. © 1999 Wiley-Liss, Inc.

The exceedingly low level of interspecific varia- Intraspecific variations in the number of cervi-
tion in the number of cervical vertebrae of mam- cal vertebrae in mammals are extremely rare,
mals has puzzled biologists for more than 150 years. whereas intraspecific variations in the number of
In birds, reptiles, and amphibians the number of more caudal vertebrae are common, especially of
cervical vertebrae varies considerably, and in mam- the lumbar, sacral, and coccygeal regions (e.g.,
mals the number of vertebrae in other vertebral Lebouck, 1898; Schulz, ’61). However, one varia-
regions is variable as well (Lebouck, 1898; Schulz, tion of cervical vertebrae does occur infrequently:
’61). Swans’ long necks have a striking 22–25 cer- cervical ribs. A cervical rib is on the seventh cer-
vical vertebrae, while ducks have 16 (Woolfenden, vical vertebra, is a partially or wholly homeotic
’61), and swifts 13 (Starck, ’79). Giraffes and drom- transformation of the seventh cervical vertebra
edaries, however, have only seven vertebrae (Fig. into the first thoracic vertebra and, thus, reduces
1), as do the Dugong (Fig. 2) and whales with their the number of cervical vertebrae (and increases
short necks (Starck, ’79). There are only three gen-
era with an exceptional number of cervical verte-
brae, manatees (Trichechus) and sloths (Bradypus
and Choloepus). Thus, there seems to be an evolu- *Correspondence to: Frietson Gailis, Institute for Evolutionary and
Ecological Sciences, University of Leiden, PO Box 9516, 2300RA
tionary constraint towards the development of vari- Leiden, The Netherlands. E-mail: Galis@rulsfb.leidenuniv.nl
ability in the cervical region in mammals. Received 28 October 1998; Accepted 16 December 1998.

© 1999 WILEY-LISS, INC.

144
20 F. GALIS

Fig. 1. Skeleton of a dromedary (Camelus dromedarius). Note the large cervical verte-
brae. From Owen (1866).

the number of thoracic vertebrae). Further study toms. Research on this syndrome has revealed that
of this naturally occurring variation seems rel- cervical ribs are invariably associated with changes
evant with respect to the evolutionary constraint in the brachial plexus (a different contribution of
on cervical vertebral number, and more specifi- motor and sensory nerves to the brachial plexus)
cally, to the study of the selective factors against and other structural abnormalities (Makhoul and
this variation. Machleder, ’92; Roos, ’96). The correlation of
symptoms must be due to mutual influences of
PATHOLOGIES ASSOCIATED WITH the notochord, neural tube, neural crest, and
CERVICAL RIBS somites at the time of somite formation (Gossler
Consideration of the pathologies in humans that and Hrabe de Angelis, ’98).
are associated with cervical ribs reveals two types, Early childhood cancer is a considerably more
thoracic outlet syndrome (TOS) and early childhood serious pathology. Childhood cancers tend to re-
cancer. TOS involves pressure on the nerves of the sult from aberrant developmental processes and
brachial plexus and on the subclavian artery, some- are generally embryonal in origin. They are asso-
times leading to severe degenerative symptoms in ciated with a high incidence of congenital abnor-
the arm (Fig. 3; Makhoul and Machleder, ’92; Roos, malities. This association is assumed to be caused
’96). Often surgery is performed to relieve symp- by a common underlying genetic abnormality

Fig. 2. Skeleton of a dugong (Dugong dugon). Note the small cervical vertebrae. From
Owen (1866).

145
 CERVICAL VERTEBRAE: HOX GENES AND CANCER 21

Fig. 3. Illustration of the thoracic outlet in a person with by permission from Adson AW. 1947. Surgical treatment for
a cervical rib showing how arteries and axons are compressed symptoms produced by cervical ribs and the scalenus anticus
when the m. anterior scalaenus contracts. The cervical rib is muscle. Surg Gynecol Obstet 85:687–700.)
incomplete and fused with the first thoracic rib. (Reproduced

(Schumacher et al., ’92; Anbazhagan and Raman, unique epidemiologic, clinical, and genetic char-
’97). A high incidence of vertebral anomalies, es- acteristics compared with cancers that occur in
pecially cervical ribs, was found in a study spe- older children. Some of the early onset cases are
cifically devoted to finding vertebral anomalies, familial cases, which are rare and generally char-
of 750 children with embryonal cancers (Schu- acterized not only by an early onset, but also by a
macher et al., ’92). An incidence of around 25% cer- worse prognosis (Brodeur, ’95; Breslow et al., ’96;
vical ribs was found for the following embryonal Gurney et al., ’96). This phenomenon is explained
cancers: neuroblastoma, brain tumour (astrocytoma by Knudson’s (’84) model for embryonal childhood
and medulloblastoma), acute lymphoblastic and cancers in which two (or only a few) mutational
myeloid leukemia, soft tissue sarcoma, Wilms’ tu- events occur before the onset of cancer. In famil-
mour and Ewing sarcoma (Table 1). This finding ial cases one of these mutations has occurred in
confirms the observations by Adson and Coffey the germ line and is transmissible to the offspring.
(’27), who found that cervical ribs are sometimes The germ-line mutation has been identified for
discovered in children because of the presence of familial retinoblastoma (reviewed in Brodeur, ’95).
a tumor in the neck. In addition, a high correla- The timing of mutational events should influence
tion between malformations of ribs (without fur- the incidence and type of congenital anomaly and
ther specification) and cancer of all types was these differences in timing can, thus, explain that
found in a large study on childhood cancers (Narod not all cases of childhood cancer have congenital
et al., ’97). defects and that the anomalies are variable.
In agreement with the hypothesis of a common
genetic abnormality underlying both early child- THE ROLE OF HOX GENES IN
hood cancer and cervical ribs is the observation PATTERNING OF THE SKELETAL AXIS
that the relation between congenital anomalies AND IN CELL PROLIFERATION
and cancer is stronger in infants than in older Hox genes play an important role in the pat-
children (Brodeur, ’95; Breslow et al., ’96; Gurney terning of the axial skeleton in all vertebrate
et al., ’96). Many infants with cancer demonstrate classes (Krumlauf, ’94). Hox gene mutants display

TABLE 1. The incidence of a cervical rib in children with embryonal cancers1

Type of childhood cancer Number of cases Incidence of a cervical rib

Neuroblastoma 88 33%
Brain tumour 234 27.4%
Leukemia 227 26.8%
Soft tissue sarcoma 98 24.5%
Wilms tumour 68 23.5%
Ewing sarcoma 35 17.1%
1
Data from Schumacher et al. (’92).

146
22 F. GALIS

abnormalities of the vertebral column. Particu- genes (Epstein et al., ’97), also display both ver-
larly common phenotypic abnormalities in mice tebral abnormalities and a predisposition for in-
mutants are cervical ribs. At least four knock-out testinal cancer (He et al., ’97). Furthermore,
mutants of hox genes in mice have an increased rostral overexpression of Hoxb-8 leads to cervical
incidence of cervical ribs (Hoxa-4, Hoxd-4, Hoxa- ribs in mice, whereas overexpression in bone mar-
5 and Hoxa-6) (reviewed in Horan et al., 95). In row is associated with leukemia (Perkins and
addition, transgenic mice overexpressing Hoxb-7 Cory, ’93) and overexpression in fibroblasts with
or Hoxb-8 and mice mutants lacking the polycomb- fibrosarcoma (a cancer) (Aberdam et al., ’91).
group genes bmi-1 and mel-18 (involved in the Thus, in mammals Hox genes are involved in
regulation of Hox genes) display cervical ribs patterning of the skeletal axis and in the prolif-
(McLain et al., ’92; Charité et al., ’94; Akasaki et eration of cell lines (among other functions) and
al., ’96; van der Lugt et al., ’96). Thus, the forma- aberrations in the regulation of Hox genes may
tion of cervical ribs is a process that seems to be lead to abnormalities in both these functions.
particularly susceptible to perturbations in Hox
gene expression (Horan et al., ’95). Most of these Selection against cervical ribs
mutant mice have a severely impaired viability. The occurrence of cervical ribs in various mam-
At the same time Hox genes have been shown malian species and the particularly frequent occur-
to be involved in the proliferation of cell lines in rence of cervical ribs in experimental mice mutants
mice and humans (e.g., Corte et al., ’93; Lawrence indicate that there is not a lack of genetic variation
et al., ’96; Anbazhagan et al., ’97). In a study in for this phenotype. Thus, there must be strong sta-
which cells of the myeloid, macrophage, erythroid, bilizing selection against the establishment of this
and B- and T-lymphoid lingeages were investi- trait. The correlated incidence of cervical ribs and
gated for expression of homeotic genes, up to 20 childhood cancer presents a strong case for ap-
different Hox genes were found to be activated parent selection against cervical ribs due to del-
(Kongsuwan et al., ’88). Some of the genes were eterious pleiotropic effects. This correlation is
ubiquitously expressed, while others were re- strengthened by the mice mutants that not only
stricted to particular cell lineages or lines (see also display variations in cervical vertebral number, but
Lawrence et al., ’96). When the cells were induced also have cancer and a much reduced fitness
to differentiate, the pattern of Hox gene expres- (Akasaki et al., ’96; van der Lugt et al., ’96;
sion changed. Changes in Hox gene expression Schumacher et al., ’96; Coré et al., ’97; He et al.,
have been demonstrated for several types of can- ’97). The incidence of cervical ribs in the general
cer, including some childhood cancers that were human population averaged over several large stud-
found to have a high incidence of vertebral anoma- ies (Adson and Coffey, ’27; Etter, ’44; Sycamore, ’44;
lies: neuroblastoma, Wilms’ tumour, and leukemia Crimm, ’52; Menárguez Carretero and Campo
(Corte et al., ’93; Lawrence et al., ’96; Manohar et Muñoz, ’67) is approximately 0.2% (347 cases out
al., ’96; Anbazhagan et al., ’97). The coupling be- of 220,026; percentages varied from 0.03–0.5). The
tween these two functions of Hox genes is clearly frequency of these embryonal cancers added to-
demonstrated in mice with mutations of the gether in the U.S. and Europe is approximately
Polycomb- and trithorax-group genes (Pc-G and 0.1% (0.01% Wilms’ tumour (15), 0.033–0.075% leu-
trx-G genes). The evolutionary-conserved Pc-G and kemia (Stiller and Parkin, ’96), 0.014% neuroblas-
trx-G genes are involved in the maintenance of toma (Gurney et al., ’96); braintumours 0.02–0.06%).
expression of homeobox genes including Hom and Assuming a chance for embryonal cancers of 0.1%
Hox genes. Mice lacking or overexpressing Pc-G and a chance for cervical ribs associated with em-
and trx-G genes have altered expression areas of bryonal cancers of 25% (Shumacher et al., ’92) im-
Hox genes and display both vertebral anomalies plies a 0.025% chance for children to have both a
(including cervical ribs and other changes in the cervical rib and early childhood cancer. Assuming a
number of cervical vertebrae) and leukemia or re- frequency of cervical ribs of 0.2% in the general
lated cancers (Corte et al., ’93; van der Lugt et al., population after early childhood and an average sur-
’94; Yu et al., ’95; Akasaki et al., ’96; Schumacher vival of 60% for early childhood cancers (Miller et
et al., ’96; Coré et al., ’97). One of these genes is the al., ’95) implies that the total incidence of cervical
trx-G gene Mll, the most commonly involved gene ribs at birth is 0.21%, of which 11.9% will develop
in infant leukemias (Pui et al., ’95). Mice heterozy- an embryonal cancer. This suggests that children
gous for the knock-out allele of the caudal gene with embryonal cancers have a 125-fold increased
Cdx2, which is involved in the regulation of Hox incidence of cervical ribs (25% vs. 0.2%), and that

147
 CERVICAL VERTEBRAE: HOX GENES AND CANCER 23

children born with a cervical rib have an almost bolic rate (McNab, ’88; Ricklefs et al., ’96). How-
120-fold chance of early childhood cancer (11.9% vs. ever, there is evidence (from canaries and pigeons)
0.1%). Thus, neonatal cancer alone seems to present that birds have a remarkably low free radical pro-
sufficient apparent selection against the establish- duction and, thus, a low amount of oxidative dam-
ment of cervical ribs. age (Perez-Campo, ’98).
In addition, the symptoms of TOS will enhance In addition, cancer in birds, especially in young
natural selection against cervical ribs by direct birds, is generally believed in the majority of cases
stabilizing selection. The seriousness of the symp- to be induced by viruses (Effron et al., ’77; Reece,
toms is correlated with the amount of manual ’96; Misdorp and Kik, personal communication).
labour that is being performed. Therefore, under In mammals viral cancers are estimated to occur
natural circumstances the selective disadvantage in 15% of cases, mainly liver cancer, cervical can-
will be larger than in the sheltered present-day cer, and Hodgkin’s disease in children (Pisani et
human environment. Adults with a rudimentary al., ’97). A survey of 343,600 young chickens
first rib (a partial transformation towards eight showed that none developed a non-virally associ-
cervical vertebrae) often have TOS, suggesting ated cancer in the first five weeks of life whereas
natural selection against this variation in cervi- 53 developed a virally associated cancer (Helmsley,
cal vertebral number as well (Gelabert et al., ’97). ’66). This pattern, confirmed by Reece (’96), is in
A further selection factor against cervical ribs striking contrast to that in human infants where
could be an increased chance of stillbirths. A large in the first month of life almost all cancers are non-
minority (>30%) of fetuses between 49 and 150 mm virally associated embryonal cancers, predomi-
has ossification centers in the seventh cervical nantly neuroblastoma (35%; Gurney et al.,’96).
prevertebra (Peters, ’27; Noback, ’51; Meyer, ’78). In reptiles the viral induction of cancer has been
These ossification centers appear in the same posi- studied much less. However, reptilian cancers
tion as those of thoracic prevertebrae’s future ribs. seem more similar to cancers in birds than in
An explanation of this phenomenon could be that mammals (Effron et al., ’77) and the viruses that
the high percentage of ossification centers (cervical induce cancer in reptiles also seem more similar
ribs) is related to the causes that have led to the to those in birds than in mammals (Trubcheninova
premature death of these fetuses. Again the inter- et al., ’77). In addition, reptiles with cancer at
active nature of the early processes which involve necropsy are usually very old, and one study has
Hox genes may present a link between cervical ribs shown that snakes with cancer are even older on
and other abnormalities, as it is unlikely that the average than snakes without cancer (Ramsay et
ossification centers themselves cause stillbirths. It al., ’96). In amphibians the situation is even less
is possible that the problems in the proliferation of well documented; however, the one type of cancer
cell lines that lead to neonatal cancer are also caus- that is well documented, Lucké’s tumour in Rana
ally related to the stillbirths. pipiens, is a virally induced cancer (McKinnell and
Carlson, ’97).
A COMPARISON OF MAMMALS, There are a few mammalian species with an ab-
REPTILES AND AMPHIBIANS errant number of cervical vertebrae: manatees and
The number of cervical vertebrae is variable in sloths. Sloths especially show a spectacular break-
amphibians, reptiles, and birds, in strong contrast down of the constraint on variation as the num-
to mammals (in fishes no cervical vertebral re- ber of cervical vertebrae varies from 6 to 9 (Giffin
gion is distinguished). The selection against such and Gillett, ’96). There is no explanation for these
variation in the number of cervical vertebrae must exceptions, but I suggest as hypothesis that the
be considerably weaker or absent in these other extremely low metabolic rate of manatees and
vertebrate classes. In necropsy studies of zoo ani- sloths (e.g., McNab ’88; Gallivan and Best ’89;
mals, cancer rates of birds and reptiles are low Koteja ’91; Hammond and Diamond, ’97) is asso-
compared to mammals (Fox, ’12; Ratcliffe, ’33; ciated with low oxidative DNA damage and, thus,
Ippen, ’59; Lombard and Witte, ’59; Effron et al., with a low susceptibility to cancer (Adelman et
’77). The low susceptibility to cancer in reptiles al., ’88; Shigenaga and Ames, ’93). This hypoth-
makes intuitive sense because of their low meta- esis needs to be tested.
bolic rate, which leads to an expectation of low
oxidative DNA damage (cf. Adelman et al., ’88; CONCLUSIONS
Perez-Campo et al., ’98). The low susceptibility in It appears, therefore, that the cause of the con-
birds may seem surprising given their high meta- servation of seven cervical vertebrae should be

148
24 F. GALIS

sought (1) in a genetic link between early child- Schilthuizen, Jan Sevenster, Elisabeth van Ast-
hood cancer and stillbirths and variation in cer- Gray, Günter Wagner, Adam Wilkins, Ole See-
vical vertebrae number, and (2) in the neuronal hausen and an anonymous referee gave many
problems leading to the thoracic outlet syndrome helpful comments on the manuscript. Thanks to
in adults associated with cervical ribs. The in- David Povel and Frank Alders for their help in
volvement of Hox genes in the cancers that are collecting literature and to Adri ’t Hooft and Mar-
associated with cervical ribs in mice and men tin Brittijn for help with the figures.
points to a coupling between functions of Hox
genes that appears to be lacking in birds, reptiles, LITERATURE CITED
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 TRABAJO PRÁCTICO 2 : EJERCITACIÓN
Problema 1.

Responda verdadero o falso y justifique TODOS los casos.
1)  La  homología  serial  a  nivel  estructural   es  un concepto  análogo  a la  duplicación  y 
divergencia   a   nivel   genético.   A   manera   de   ejemplo,   se   asume   que   a   partir   de   una 
vértebra   ancestral  se generó   un  mayor  número  de vértebras  en  los   taxa   derivados   a 
través de su duplicación, y análogamente el origen de una familia multigénica de varios 
genes   parálogos   a   través   de   la   duplicación   de   un   gen   ancestral   con   la   posterior 
divergencia.
2) Las heterocronías son cambios en el tiempo de desarrollo de una estructura dada en 
diferentes   taxa.   Es   decir   que,   si   dos   grupos   hermanos   tienen   el   mismo   tiempo   de 
desarrollo de la estructura estudiada, no hubo procesos heterocrónicos a lo largo de la 
evolución del linaje.
3) La ontogenia recapitula la filogenia.

Problema 2.

La evolución de los apéndices es uno de los temas más estudiados bajo una perspectiva 
filogenética,   de   embriología   comparada   y   experimental.   En   particular   dentro   de   los 
tetrápodos, los anfibios son un grupo de gran diversidad en cuanto al número de dígitos 
y falanges. 
Entre   los   anfibios,   existen   dos   grandes   órdenes:   los  Anuros  (ranas)   y   los  Urodelos 
(salamandras),   ambos,   por   lo   general,   poseen   5   dígitos   en   sus   apéndices   posteriores. 
Diferentes   estudios   sugieren  que  el   ancestro  de estos   dos  grupos   poseía   un  apéndice 
posterior   caracterizado   por   2   falanges   en   el   primer   dígito,   3   en   el   segundo,   4   en   el 
tercero, 4 en el cuarto y 3 en el quinto (formula del número de falanges: 2­3­4­4­3). 
Por lo general, las especies de Anuros son muy conservadas en el número de falanges 
con   una   fórmula   de   falanges   de   2­2­3­4­3   (ver   Figura   1).   Por   el   contrario,   en   los 
Urodelos la fórmula del número de falanges es mucho más variable que en los Anuros. 

153
En la Tabla I se esquematiza la secuencia de diferenciación de las falanges durante la 
ontogenia   en   dos   especies   modelo  Xenopus   laevis  y  Ambystoma   mexicanus,   anuro   y 
urodelo, respectivamente. De acuerdo a esta información:
2.1. ¿es sincrónico el desarrollo de los dígitos en cada especie? 
2.2. ¿Qué clase de homología está implícita en esta comparación? Defínala.

154
Pere Alberch, gran embriólogo evolutivo, abordó de manera experimental el problema de 
la variación en el número de falanges en los anfibios, tratando con un inhibidor mitótico 
(colchicina) durante las etapas tempranas del desarrollo de los apéndices posteriores de 
ambas   especies.  Como  resultado  de  este  experimento  se observó  una   reducción   en  el 
número   de   falanges   en   los   5   dígitos   de   cada   especie.   La   información   de   dicho 
experimento se resume en las Figuras 1 y 2. 
2.3.  ¿Encuentra algún tipo de patrón que relacione la reducción del número de 
dígitos   con   el   tiempo   de   desarrollo   de   los   mismos?   Formule   una   hipótesis   que 
vincule ambos resultados.

En la naturaleza se puede observar especies de anfibios con 4 dedos, tanto en el orden de 
los Anuros como en el de los Urodelos. Tal es el caso de la especie Psyllophryne didactyla  
(Anuros)   cuya   fórmula   de   numero   de   falanges   es:   0­2­3­4­1,   como   la   especie 
Salamandrina terdigitata (Urodelo) cuya fórmula es de: 1­2­3­2­0. Si este patrón natural 
concuerda con la hipótesis planteada anteriormente por Ud.:
2.4.  ¿El   dedo   “pulgar”   (el   primer   dígito   con   falange)   de   ambas   especies   es 
homólogo (primario)? Justifique su respuesta utilizando los criterios de homología. 
Defina los términos alometría evolutiva y alometría ontogenética e identifique un 
ejemplo de ambos en el caso de estudio.

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Problema 3.
Las alas son una adaptación muy importante de los insectos, la cual les permite escapar 
de los predadores, explotar recursos y dispersarse a nuevos nichos. Pese a las supuestas 
ventajas evolutivas de las alas, casi todos los órdenes de insectos alados poseen linajes 
con   reducción   parcial   o   total   de   las   alas.   En   este   sentido,   cientos   de   transiciones 
independientes de formas aladas a no aladas han ocurrido durante la evolución de las 
alas. Sin embargo, una reversión de una forma sin alas a una con alas nunca ha sido 
demostrada   claramente,   dado   que   tal   reversión   sería   muy   improbable   dadas   las 
complejas interacciones entre nervios, músculos, y escleritos que se requieren para el 
vuelo.
3.1. Bajo esta hipótesis inicial: ¿son homólogas las alas de los distintos insectos? ¿Y 
el primer y segundo par dentro de cada especie? Indique que información utilizaría 
para   estudiar   alometrías   estáticas,   ontogenéticas   y   evolutivas   del   ala   dentro   de 
algún género en particular. 
3.2. Un estudio reciente de la evolución de las alas dentro del orden Phasmatodea 
(los llamados “bichos palo”) mostró el siguiente resultado:

Grupos externos

Referencias. Estrella: ganancia de alas. Triángulo: pérdida de alas. Circulo vacío: 
especies con alas.

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 ¿Modifica este resultado su respuesta anterior? Justifique.

3.3. Un tercer estudio mostró que los genes involucrados en el patrón de desarrollo 
de las alas están presentes en todos los insectos, incluso los ápteros. Proponga una 
hipótesis para explicar este resultado y (de ser necesario) reconciliar las hipótesis 
anteriores. 

Problema 4.
Adams y Nistri (BMC Evolutionary Biology 2010) estudiaron la morfología de las patas 
de ocho especies de salamandras europeas del género Hydromantes para poner a prueba 
la hipótesis de que la morfología del adulto constituye una adaptación relacionada con 
sus hábitos arborícolas. Estos autores observaron que cinco especies habitantes de la isla 
de  Cerdeña   alcanzan  un   tamaño  mayor   que  las   otras   tres   especies   pertenecientes   al 
continente. Sin embargo, todas las especies muestran valores similares y relativamente 
bajos de sinuosidad lo que implica la presencia de más tejido interdigital (Fig. 1).

Figura   1:  Esquemas   de   la   pata   de   las   salamandras   estudiadas   que   muestran   la   mayor 
sinuosidad y menor presencia de tejido interdigital en individuos pequeños (a la izquierda) en 
comparación con individuos grandes (a la derecha).

Cuando estos autores analizaron la morfología a lo largo del desarrollo de cada especie, 
encontraron patrones muy diferentes (Tabla 1). Por un lado, la mayoría de la especies no 
mostró cambios en el nivel de sinuosidad (o en la abundancia de tejido interdigital) a 
través de la ontogenia. Por otro lado, en tres especies habitantes de la isla, se observó 
que el nivel de sinuosidad disminuye (o que la cantidad de tejido interdigital aumenta) a  
medida que los animales crecen.

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Tabla 1:  Principales resultados de los análisis de regresión de la sinuosidad versus el tamaño 
total.   Para   cada   especie   se   muestra   el   valor   de   la   pendiente   de   la   recta   de   regresión   y   la 
significación asociada. p < 0,05 indicado en negrita, c: especie continental, i: especie isleña.

a)  Interprete   los   resultados   de   la   Tabla   1.   Identifique   el/los   tipo/s   de   alometría/s 

analizados.
A continuación, para comprender mejor la evolución de las trayectorias ontogenéticas 
analizadas, los autores utilizaron una filogenia del grupo y encontraron que el patrón de 
independencia   entre   caracteres   es   el   estado   ancestral   más   probable   para   el   linaje 
europeo (Fig. 2).

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Figura 2: Relaciones filogenéticas de las especies de salamandras europeas estudiadas basadas 
en   una   filogenia   molecular   realizada   utilizando   datos   de   secuencias   de   ADN   mitocondrial   y 
nuclear.   Los   esquemas   muestran   el   patrón   de   alometría   asociado   a   cada   especie.   c:   especie 
continental, i: especie isleña.

b)  En base a estos resultados, ¿qué conclusiones puede extraer acerca de la homología 
del   patrón   de   crecimiento   alométrico   observado   en   las   tres   especies   isleñas?   ¿Cómo 
podría explicar estos resultados considerando el concepto de heterocronía?

Posteriormente,  se  estudió   la   trayectoria   ontogenética  de   una  especie  de   salamandra 
norteamericana (H. platycephalus) la cual exhibe un crecimiento alométrico similar al 
observado en las especies isleñas. Cuando se incluyó a  H. platycephalus  en el análisis, 
los patrones descriptos anteriormente no cambiaron pero si lo hizo la condición ancestral 
de todo el género la cual pasó a ser alométrica.
c)  ¿Modifica este resultado su hipótesis de homología expuesta en el punto anterior? 
Justifique.

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Finalmente,   los   autores   extendieron   estos   análisis   a   más   especies   de   salamandras 
pertenecientes a otros géneros y observaron que las trayectorias ontogenéticas de las 
especies europeas se asemejan, por un lado, a especies que poseen hábitos similares (es 
decir, especies trepadoras) y, por otro lado, a especies cavadoras las cuales presentan 
una posición más basal en la filogenia de las salamandras.
d) ¿Cómo podría explicar estos resultados en términos de exaptación?

Problema 5.
Relacione cada uno de los siguientes gráficos con uno de los enunciados a continuación. 
Justifique sus respuestas.
a.  El   estudio   comparado  de   las   alometrías   a   nivel   craneofacial   no   permite  inferir 
procesos heterocrónicos dado que en la muestra se hallan subrepresentados algunos 
estadios   ontogenéticos   de   ambas   especies.   También   se   sospecha   que   una   de   las 
muestras ontogenéticas incluye ejemplares de más de una especie.
b.  Un   proceso   heterocrónico   de   tipo   pedomórfico   actuó   a   nivel   craneofacial   en 
humanos mientras que no se puede postular un cambio en los tiempos de desarrollo 
de dichas estructuras en chimpancés.
c.  La   relación  entre   la   forma   del   neurocráneo   y  la  forma  de   la   cara   en   humanos 
presenta un desarrollo desacelerado desde la adolescencia a la adultez con respecto a 
estadios anteriores de su ontogenia.
d.  El   estudio   de   las   alometrías   a   nivel   craneofacial   no   permite   inferir   procesos 
heterocrónicos en la divergencia entre los linajes de humanos y chimpancés.
e.  Nuestra  especie se caracteriza  por  una  acentuada  aceleración  de los  ritmos  de 
desarrollo.

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 MÓDULO VIII

MACROEVOLUCIÓN
 

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 TRABAJO PRÁCTICO N° 1
MACROEVOLUCIÓN
NIVELES EN LOS SISTEMAS COMPLEJOS
Sobre los niveles, sus límites y Borges

INTRODUCCIÓN GENERAL

“Todos estamos familiarizados con la [clase de cosas que pueden ser comprendidas en
diferentes niveles]. Sin embargo, por algún motivo algunos de ellos nos resultan más fáciles de
imaginar e integrar a nuestra vida cotidiana o a nuestro conocimiento sin que ello nos ocasiones
mayores inconvenientes. (…) Por ejemplo, todos sabemos que los seres humanos están
integrados por una enorme cantidad de células (veinticinco trillones, aproximadamente), y que,
en consecuencia, todo lo que hacemos podría estar descrito, en principio, en función celular. O
bien la descripción podría hacerse, inclusive, en el nivel de las moléculas. La mayoría de nosotros
acepta esto de una manera bastante limitada; vamos al médico para que examine lo que
consideramos nuestros niveles inferiores. Leemos sobre el ADN y la “ingeniería genética” y
sorbemos nuestro café. Pareciera que hemos conciliado estas dos imágenes increíblemente
distintas de nosotros mismos mediante el simple recurso de desconectarlas entre sí. No contamos
prácticamente con ninguna forma de relacionar una descripción microscópica de nosotros mismos
con lo que imaginamos que somos, y de ahí que sea posible el almacenamiento de
representaciones disociadas de nosotros mismos en “compartimientos” de nuestra mente
disociados por completo entre sí. Rara vez nos vemos en situación de alternar entre uno y otro de
estos conceptos, preguntándonos, “¿cómo estas dos cosas totalmente diferentes pueden ser el
mismo yo?””.

Fragmento extraído del libro “Gödel, Escher, Bach, un eterno y grácil bucle” de Hofstadter (pág. 316)

OBJETIVOS

• Aplicar el concepto de niveles y sus características a un caso biológico.

• Que el alumno comprenda las posiciones denominadas emergentistas y reduccionistas en el
marco de los debates evolutivos.
• Identificar las diferencias entre macro y microevolución tanto a nivel del objeto de estudio
como de los mecanismos subyacentes.

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PRIMERA PARTE: El debate sobre la unicidad o la multiplicidad de niveles
Lea atentamente el texto Furmiga, fragmento seleccionado y adaptado correspondiente al
Capítulo X del libro: “Gödel, Escher, Bach: un eterno y grácil bucle” de Douglas Hofstadter.
Responda:
1.1 ¿Qué se entiende por “holismo”? ¿Qué por “reduccionismo”?
1.2. ¿Qué son los niveles de un sistema según el autor?
1.3 ¿Pueden tener diferentes propiedades estos niveles? ¿Pueden los sistemas estar
correlacionados entre sí a distintos niveles u operar procesos similares a distintos niveles?
Analice los casos presentados por Hofstadter.

SEGUNDA PARTE: El debate sobre la unicidad o la multiplicidad de niveles

Lea atentamente el artículo “El Darwinismo y La Expansión de la Teoría de la Evolución” de S.J.
Gould, 1983, Interciencia (8)3:143-151. (Traducción al español del artículo “Darwinism and the
expansion of the evolutionary theory” Science 216:380-387).
Responda:
2.1. ¿Qué es el Darwinismo para Gould y cuáles son sus postulados centrales y periféricos?
2.2. Sintetice las críticas de Gould al Darwinismo.
2.3. Sobre el origen histórico de las estructuras:
¿Cuáles son las críticas al concepto clásico de adaptación? ¿Qué importancia le da
Gould a las “no-adaptaciones”?
¿Qué son las exaptaciones?
2.4. Sobre los patrones macroevolutivos:
¿Qué propone la teoría de Equilibrios Puntuados?
2.5. Sobre los procesos macroevolutivos:
¿Qué es la selección de especies?
¿Qué condiciones deberían cumplirse para definirla como tal?
¿Usted cree que Gould es realista o instrumentalista cuando habla de las especies?
Justifique.
¿Cuáles son los niveles sobre los que podrían actuar la selección según Gould?
Identifíquelos en el texto.
2.6. Sobre su propuesta:
¿Cómo considera Gould que debería ser una teoría evolutiva basada en una concepción
jerárquica de la evolución?

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TERCERA PARTE: El debate sobre la unicidad o la multiplicidad de niveles
Lea atentamente los fragmentos seleccionados del artículo “Acquiring Genomes: A Theory of the
Origins of Species” de L. Margulis & D. Sagan, 2002, Perseus Books Group (traducidos al
español).
Responda:
3.1. ¿Qué entienden Magulis y Sagan por simbiosis? ¿Qué por simbiogénesis? ¿Considera
Ud. que éstas son fuerzas evolutivas de importancia? ¿Por qué?
3.2. ¿Cuál es la crítica que realizan Margulis y Sagan al concepto biológico de especie?
¿Cree Ud. que esta crítica puede ser salvada utilizando otro concepto de especie tal
como los que ha visto anteriormente?
3.3. a) ¿Cuál es la crítica de Margulis al concepto de “competencia”? ¿Qué alcances
empíricos tiene dicho concepto según los autores?
b) ¿Dónde radica según los autores este “olvido” de la teoría de la simbiogénesis como
fuerza evolutiva? ¿Qué cree Ud. al respecto? Responda relacionando lo anterior con lo
visto en el primer práctico de la materia acerca de factores internos y externos.

CUARTA PARTE (ADICIONAL): Estudio de los límites de los niveles: un abordaje

borgeano

Lea atentamente los cuentos propuestos de J. L. Borges y responda:

4.1. Texto: “Funes, el memorioso”

- ¿Qué significa la frase borgeana “pensar es abstraer
diferencias”?
- ¿Cuál es la ventaja y cuál es la desventaja gnoseológica (del
conocimiento)?

4.2. Texto: “El Idioma Analítico de John Wilkins”

- ¿Qué problemas aparentes arroja la clasificación de la Enciclopedia China?
- ¿Cómo se elige el criterio para una clasificación? ¿Qué implicancias puede tener dicha
elección?
4.3. Texto: “Del rigor en la ciencia”

- Relacione este cuento con el problema planteado en “Funes, el memorioso”. ¿En qué
sentido esta historia se relaciona con el “olvidar diferencias” de Funes?
- ¿Qué conclusiones generales se obtienen del cuento?
4.4. Utilizando los tres cuentos simultáneamente, ¿qué relación cree Ud. que tiene todo esto
con la Teoría de la Evolución?

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 El libro Ficciones, escrito por Jorge Luis Borges, Italia, Alemania y España.
incluye una serie de cuentos que pertenecen “a Uno de los cuentos que relata y que
la clásica categoría de las piezas antológicas”. reproducimos en esta edición de Petrotecnia es
Traducido a varios idiomas, fue galardonado en “Funes el memorioso” que, según el propio
1961 con el Premio Internacional otorgado por autor, “es una larga metáfora del insomnio”.
editores de Francia, Estados Unidos, Inglaterra,

Una ventana cultural

Funes el memorioso
Por Jorge Luis Borges
Se agradece a la Fundación Internacional Jorge Luis Borges el permiso para su publicación. © María Kodama

L
o recuerdo (yo no tengo derecho a pronunciar ese
verbo sagrado, sólo un hombre en la tierra tuvo
derecho y ese hombre ha muerto) con una oscura
pasionaria en la mano, viéndola como nadie la ha visto,
aunque la mirara desde el crepúsculo del día hasta el de la
noche, toda una vida entera. Lo recuerdo, la cara taciturna y
aindiada y singularmente remota, detrás del cigarrillo.
Recuerdo (creo) sus manos afiladas de trenzador. Recuerdo
cerca de esas manos un mate, con las armas de la Banda
Oriental; recuerdo en la ventana de la casa una estera amari-
lla, con un vago paisaje lacustre. Recuerdo claramente su
voz; la voz pausada, resentida y nasal del orillero antiguo,
sin los silbidos italianos de ahora. Más de tres veces no lo vi;
la última, en 1887... Me parece muy feliz el proyecto de que
todos aquellos que lo trataron escriban sobre él; mi testimo-
nio será acaso el más breve y sin duda el más pobre, pero no
el menos imparcial del volumen que editarán ustedes.
Mi deplorable condición de argentino me impedirá incu-
rrir en el ditirambo –género obligatorio en el Uruguay, cuan-
do el tema es uruguayo. Literato, cajetilla, porteño; Funes nos
dijo esas injuriosas palabras, pero de un modo suficiente me
consta que yo representaba para él esas desventuras. Pedro
Leandro Ipuche ha escrito que Funes era un precursor de los
superhombres, “un Zarathustra cimarrón y vernáculo”; no lo
discuto, pero no hay que olvidar que era también un compa-
drito de Fray Bentos, con ciertas incurables limitaciones.
Mi primer recuerdo de Funes es muy perspicuo. Lo veo
en un atardecer de marzo o febrero del año ochenta y cua-
tro. Mi padre, ese año, me había llevado a veranear a Fray
Bentos. Yo volvía con mi primo Bernardo Haedo de la
estancia de San Francisco. Volvíamos cantando, a caba-
llo, y ésa no era la única circunstancia de mi felicidad.
Después de un día bochornoso, una enorme tormenta
color pizarra había escondido el cielo. La alentaba el
viento del Sur, ya se enloquecían los árboles; yo tenía
el temor (la esperanza) de que nos sorprendiera en un
descampado el agua elemental. Corrimos una especie de
carrera con la tormenta. Entramos en un callejón que se
ahondaba entre dos veredas altísimas de ladrillo.
Había oscurecido de golpe; oí rápidos y casi secretos
pasos en lo alto; alcé los ojos y vi un muchacho que corría
Esta imagen fue realizada en 1976, por el prestigioso ilustrador
argentino Osavaldo Pérez D’Elías (hoy residiendo en España) para la por la estrecha y rota vereda como por una estrecha y rota
revista Temas de Petroquímica General Mosconi. pared. Recuerdo la bombacha, las alpargatas, recuerdo el

94 I Petrotecnia • junio, 2004 195

cigarrillo en el duro rostro, contra el nubarrón ya sin lími- El catorce de febrero me telegrafiaron de Buenos Aires que
tes. Bernardo le gritó imprevisiblemente: ¿Qué hora son volviera inmediatamente, porque mi padre no estaba “nada
Ireneo? Sin consultar el cielo, sin detenerse, el otro res- bien”. Dios me perdone; el prestigio de ser el destinatario de
pondió: Faltan cuatro minutos para las ocho, joven un telegrama urgente, el deseo de comunicar a todo Fray
Bernardo Juan Francisco. La voz era aguda, burlona. Bentos la contradicción entre la forma negativa de la noticia
Yo soy tan distraído que el diálogo que acabo de referir y el perentorio adverbio, la tentación de dramatizar mi
no me hubiera llamado la atención si no lo hubiera recal- dolor, fingiendo un viril estoicismo, tal vez me distrajeron
cado mi primo, a quien estimulaban (creo) cierto orgullo de toda posibilidad de dolor. Al hacer la valija, noté que me
local, y el deseo de mostrarse indiferente a la réplica tri- faltaba el Gradus y el primer tomo de la Naturalis historia. El
partita del otro. “Saturno” zarpaba al día siguiente, por la mañana; esa
Me dijo que el muchacho del callejón era un tal Ireneo noche, después de cenar, me encaminé a casa de Funes. Me
Funes, mentado por algunas rarezas como la de no darse asombró que la noche fuera no menos pesada que el día.
con nadie y la de saber siempre la hora, como un reloj. En el decente rancho, la madre de Funes me recibió.
Agregó que era hijo de una planchadora del pueblo, María Me dijo que Ireneo estaba en la pieza del fondo y que no
Clementina Funes, y que algunos decían que su padre era me extrañara encontrarla a oscuras, porque Ireneo sabía
un médico del saladero, un inglés O’Connor, y otros un pasarse las horas muertas sin encender la vela. Atravesé el
domador o rastreador del departamento del Santo. Vivía patio de baldosa, el corredorcito; llegué al segundo patio.
con su madre, a la vuelta de la quinta de los Laureles. Había una parra; la oscuridad pudo parecerme total. Oí de
Los ochenta y cinco y ochenta y seis veraneamos en la pronto la alta y burlona voz de Ireneo. Esa voz hablaba en
ciudad de Montevideo. El ochenta y siete volví a Fray latín; esa voz (que venía de la tiniebla) articulaba con moroso
Bentos. Pregunté, como es natural, por todos los conocidos deleite un discurso o plegaria o incantación. Resonaron las
y, finalmente, por el “cronométrico Funes”. Me contestaron sílabas romanas en el patio de tierra; mi temor las creía indes-
que lo había volteado un redomón en la estancia de San cifrables, interminables; después, en el enorme diálogo de esa
Francisco, y que había quedado tullido, sin esperanza. noche, supe que formaban el primer párrafo del vigésimo-
Recuerdo la impresión de incómoda magia que la noticia me cuarto capítulo del libro séptimo de la Naturalis historia. La
produjo: la única vez que yo lo vi, veníamos a caballo de materia de ese capítulo es la memoria; las palabras últimas
San Francisco y él andaba en un lugar alto; el hecho, en fueron ut nihil non iisdem verbis redderetur auditum.
boca de mi primo Bernardo, tenía mucho de sueño elabora- Sin el menor cambio de voz, Ireneo me dijo que pasa-
do con elementos anteriores. Me dijeron que no se movía ra. Estaba en el catre, fumando. Me parece que no le vi la
del catre, puestos los ojos en la higuera del fondo o en una cara hasta el alba; creo rememorar el ascua momentánea
telaraña. En los atardeceres, permitía que lo sacaran a la ven- del cigarrillo. La pieza olía vagamente a humedad. Me
tana. Llevaba la soberbia hasta el punto de simular que era senté; repetí la historia del telegrama y de la enfermedad
benéfico el golpe que lo había fulminado... Dos veces lo vi de mi padre.
atrás de la reja, que burdamente recalcaba su condición de Arribo, ahora, al más difícil punto de mi relato. Éste
terno prisionero: una, inmóvil, con los ojos cerrados; otra, (bueno es que ya lo sepa el lector) no tiene otro argumen-
inmóvil también, absorto en la contemplación de un oloro- to que ese diálogo de hace ya medio siglo. No trataré de
so gajo de santonina. reproducir sus palabras, irrecuperables ahora. Prefiero resu-
No sin alguna vanagloria yo había iniciado en aquel mir con veracidad las muchas cosas que me dijo Ireneo. El
tiempo el estudio metódico del latín. Mi valija incluía el estilo indirecto es remoto y débil; yo sé que sacrifico la efi-
De viris illustribus de Lhomond, el Thesaurus de Quicherat, cacia de mi relato; que mis lectores se imaginen los entre-
los comentarios de Julio César y un volumen impar de la cortados períodos que me abrumaron esa noche.
Naturalis historia de Plinio, que excedía (y sigue excedien- Ireneo empezó por enumerar, en latín y español, los
do) mis módicas virtudes de latinista. Todo se propala en casos de memoria prodigiosa registrados por la Naturalis
un pueblo chico; Ireneo, en su rancho de las orillas, no historia; Ciro, rey de los persas, que sabía llamar por su
tardó en enterarse del arribo de esos libros anómalos. Me nombre a todos los soldados de sus ejércitos; Mitríades
dirigió una carta florida y ceremoniosa, en la que recordaba Eupator, que administraba la justicia en los 22 idiomas de
nuestro encuentro, desdichadamente fugaz, “del siete de su imperio; Simónides, inventor de la mnemotecnia;
febrero del ochenta y cuatro”, ponderaba los gloriosos ser- Metrodoro, que profesaba el arte de repetir con fidelidad
vicios que don Gregorio Haedo, mi tío, finado ese mismo lo escuchado una sola vez. Con evidente buena fe se mara-
año, “había prestado a las dos patrias en la valerosa jornada villó de que tales casos maravillaran. Me dijo que antes de
de Ituzaingó”, y me solicitaba el préstamo de cualquiera de esa tarde lluviosa en que lo volteó el azulejo, él había sido
los volúmenes, acompañado de un diccionario “para la lo que son todos los cristianos: un ciego, un sordo, un
buena inteligencia del texto original, porque todavía ignoro abombado, un desmemoriado. (Traté de recordarle su per-
el latín”. Prometía devolverlos en buen estado, casi inme- cepción exacta del tiempo, su memoria de nombres pro-
diatamente. La letra era perfecta, muy perfilada; la ortogra- pios; no me hizo caso.) Diez y nueve años había vivido
fía del tipo que Andrés Bello preconizó: i por y, j por g. Al como quien sueña: miraba sin ver, oía sin oír, se olvidaba
principio, temí naturalmente una broma. Mis primos me de todo, de casi todo. Al caer, perdió el conocimiento;
aseguraron que no, que eran cosas de Ireneo. No supe si cuando lo recobró, el presente era casi intolerable de tan
atribuir a descaro, a ignorancia o a estupidez la idea de que rico y tan nítido, y también las memorias más antiguas y
el arduo latín no requería más instrumento que un diccio- más triviales. El hecho apenas le interesó. Razonó (sintió)
nario; para desengañarlo con plenitud le mandé el Gradus que la inmovilidad era un precio mínimo. Ahora su per-
ad Parnassum de Quicherar y la obra de Plinio. cepción y su memoria eran infalibles.

196 Petrotecnia • junio, 2004 I 95

 Nosotros, de un vistazo, percibimos tres copas en una cifras. Lo disuadieron dos consideraciones: la conciencia de
mesa; Funes, todos los vástagos y racimos y frutos que que la tarea era interminable, la conciencia de que era
comprende una parra. Sabía las formas de las nubes aus- inútil. Pensó que en la hora de la muerte no habría acabado
trales del amanecer del treinta de abril de mil ochocientos aún de clasificar todos los recuerdos de la niñez.
ochenta y dos y podía compararlas en el recuerdo con las Los dos proyectos que he indicado (un vocabulario infi-
vetas de un libro en pasta española que sólo había mirado nito para la serie natural de los números, un inútil catálogo
una vez y con las líneas de la espuma que un remo levan- mental de todas la imágenes del recuerdo) son insensatos,
tó en el Río Negro la víspera de la acción del Quebracho. pero revelan cierta balbuciente grandeza. Nos dejan vis-
Esos recuerdos no eran simples; cada imagen visual estaba lumbrar o inferir el vertiginoso mundo de Funes. Éste, no
ligada a sensaciones musculares, térmicas, etc. Podía lo olvidemos, era casi incapaz de ideas generales, platóni-
reconstruir todos los sueños, todos los entresueños. Dos o cas. No sólo le costaba comprender que el símbolo genéri-
tres veces había reconstruido un día entero; no había co perro abarcara tantos individuos dispares de diversos
dudado nunca, pero cada reconstrucción había requerido tamaños y diversa forma; le molestaba que el perro de las
un día entero. Me dijo: Más recuerdos tengo yo solo que tres y catorce (visto de perfil) tuviera el mismo nombre que
los que habrán tenido todos los hombres desde que el el perro de las tres y cuarto (visto de frente). Su propia cara
mundo es mundo. Y también: Mis sueños son como la en el espejo, sus propias manos, lo sorprendían cada vez.
vigilia de ustedes. Y también, hacia el alba: Mi memoria, Refiere Swift que el emperador de Lilliput discernía el
señor, es como vaciadero de basuras. Una circunferencia movimiento del minutero; Funes discernía continuamente
en un pizarrón, un triángulo rectángulo, un rombo, son los tranquilos avances de la corrupción, de las caries, de la
formas que podemos intuir plenamente; lo mismo le pasa- fatiga. Notaba los progresos de la muerte, de la humedad.
ba a Ireneo con las aborrascadas crines de un potro, con Era el solitario y lúcido espectador de un mundo multifor-
una punta de ganado en una cuchilla, con el fuego cam- me, instantáneo y casi intolerablemente preciso. Babilonia,
biante y con la innumerable ceniza, con las muchas caras Londres y Nueva York han abrumado con feroz esplendor
de un muerto en un largo velorio. No sé cuántas estrellas la imaginación de los hombres; nadie, en sus torres popu-
veía en el cielo. losas o en sus avenidas urgentes, ha sentido el calor y la
Esas cosas me dijo; ni entonces ni después las he puesto presión de una realidad tan infatigable como la que día y
en duda. En aquel tiempo no había cinematógrafos ni fonó- noche convergía sobre el infeliz Ireneo, en su pobre arrabal
grafos; es, sin embargo, inverosímil y hasta increíble que sudamericano. Le era muy difícil dormir. Dormir es dis-
nadie hiciera un experimento con Funes. Lo cierto es que traerse del mundo; Funes, de espaldas en el catre, en la
vivimos postergando todo lo postergable; tal vez todos sabe- sombra, se figuraba cada grieta y cada moldura de las casas
mos profundamente que somos inmortales y que tarde o precisas que lo rodeaban. (Repito que el menos importante
temprano, todo hombre hará todas las cosas y sabrá todo. de sus recuerdos era más minucioso y más vivo que nuestra
La voz de Funes, desde la oscuridad, seguía hablando. percepción de un goce físico o de un tormento físico.)
Me dijo que hacia 1886 había discurrido un sistema ori- Hacia el Este, en un trecho no amanzanado, había casas
ginal de numeración y que en muy pocos días había reba- nuevas, desconocidas. Funes las imaginaba negras, compac-
sado el veinticuatro mil. No lo había escrito, porque lo tas, hechas de tiniebla homogénea; en esa dirección volvía
pensado una sola vez ya no podía borrársele. Su primer la cara para dormir. También solía imaginarse en el fondo
estímulo, creo, fue el desagrado de que los treinta y tres del río, mecido y anulado por la corriente.
orientales requirieran dos signos y tres palabras, en lugar Había aprendido sin esfuerzo el inglés, el francés, el
de una sola palabra y un solo signo. Aplicó luego ese dis- portugués, el latín. Sospecho, sin embargo, que no era
paratado principio a los otros números. En lugar de siete muy capaz de pensar. Pensar es olvidar diferencias, es
mil trece, decía (por ejemplo) Máximo Pérez; en lugar de generalizar, abstraer. En el abarrotado mundo de Funes no
siete mil catorce, El Ferrocarril; otros números eran Luis había detalles, casi inmediatos.
Melián Lafinur, Olimar, azufre, los bastos, la ballena, el La recelosa claridad de la madrugada entró por el patio
gas, la caldera, Napoleón, Agustín de Vedia. En lugar de de tierra.
quinientos, decía nueve. Cada palabra tenía un signo par- Entonces vi la cara de la voz que toda la noche había
ticular, una especie de marca; las últimas eran muy com- hablado. Ireneo tenía diecinueve años; había nacido en
plicadas...Yo traté de explicarle que esa rapsodia de voces 1868; me pareció monumental como el bronce, más anti-
inconexas era precisamente lo contrario de un sistema de guo que Egipto, anterior a las profecías y a las pirámides.
numeración. Le dije que decir 365 era decir tres centenas, Pensé que cada una de mis palabras (que cada uno de mis
seis decenas, cinco unidades; análisis que no existe en los gestos) perduraría en su implacable memoria; me entorpe-
“números” El Negro Timoteo o manta de carne. Funes no ció el temor de multiplicar ademanes inútiles.
me entendió o no quiso entenderme. Ireneo Funes murió en 1889, de una congestión pulmonar. .
Locke, en el siglo XVII, postuló (y reprobó) un idioma
imposible en el que cada cosa individual, cada piedra, cada

1942
pájaro y cada rama tuviera un nombre propio; Funes pro-
yectó alguna vez un idioma análogo, pero lo desechó por
parecerle demasiado general, demasiado ambiguo. En efec-
to, Funes no sólo recordaba cada hoja de cada árbol de cada
monte, sino cada una de las veces que la había percibido o
imaginado. Resolvió reducir cada una de sus jornadas preté-
ritas a unos setenta mil recuerdos, que definiría luego por

96 I Petrotecnia • junio, 2004 197

 1/3
EL IDIOMA ANALÍTICO
DE JOHN WILKINS

Otras inquisiciones, Jorge Luis Borges, EMECÉ 1996.

HE COMPROBADO que la décimocuarta edición de la Encyc1opaedia Britannica suprime el artículo

sobre John Wilkins. Esa omisión es justa, si recordamos la trivialidad del artículo (veinte renglones
de meras circunstancias biográficas: Wilkins nació en 1614, Wilkins murió en 1672, Wilkins fue
capellán de Carlos Luis, príncipe palatino; Wilkins fue nombrado rector de uno de los colegios de
Oxford, Wilkins fue el primer secretario de la Real Sociedad de Londres, etcétera); es culpable, si
consideramos la obra especulativa de Wilkins. Éste abundó en felices curiosidades: le interesaron la
teología, la criptografía, la música, la fabricación de colmenas transparentes, el curso de un planeta
invisible, la posibilidad de un viaje a la luna, la posibilidad y los principios de un lenguaje mundial.
A este último problema dedicó el libro An Essay towards a Real Character and a Philosophical
Language (600 páginas en cuarto mayor, 1668). No hay ejemplares de este libro en nuestra
Biblioteca Nacional; he interrogado, para redactar esta nota, The Life and Times of John Wilkins
(1910), de P. A. Wright Henderson; el Woerterbuch der Phílosophie (1924), de Fritz Mauthner;
Delphos (1935), de E. Sylvia Pankhurst; Dangerous Thoughts (1939), de Lancelot Hogben.

Todos, alguna vez, hemos padecido esos debates inapelables en que una dama, con acopio de
interjecciones y de anacolutos, jura que la palabra luna es más (o menos) expresiva que la palabra
moon. Fuera de la evidente observación de que el monosílabo moon es tal vez más apto para
representar un objeto muy simple que la palabra bisilábica luna, nada es posible contribuir a tales
debates; descontadas las palabras compuestas y las derivaciones, todos los idiomas del mundo (sin
excluir el volapük de Johann Martin Schleyer y la romántica interlingua de Peano) son igualmente
inexpresivos. No hay edición de la Gramática de la Real Academia que no pondere “el envidiado
tesoro de voces pintorescas, felices y expresivas de la riquísima lengua española”, pero se trata de
una mera jactancia, sin corroboración. Por lo pronto, esa misma Real Academia elabora cada tantos
años un diccionario, que define las voces del español… En el idioma universal que ideó Wilkins al
promediar el siglo XVII, cada palabra se define a sí misma. Descartes, en una epístola fechada en
noviembre de 1629, ya había anotado que mediante el sistema decimal de numeración, podemos
aprender en un solo día a nombrar todas las cantidades hasta el infinito y a escribirlas en un idioma
nuevo que es el de los guarismos1; también había propuesto la formación de un idioma análogo,
general, que organizara y abarcara todos los pensamientos humanos. John Wilkins, hacia 1664,
acometió esa empresa.

Dividió el universo en cuarenta categorías o géneros, subdivisibles luego en diferencias,

subdivisibles a su vez en especies. Asignó a cada género un monosílabo de dos letras; a cada
diferencia, una consonante; a cada especie, una vocal. Por ejemplo: de, quiere decir elemento; deb,
el primero de los elementos, el fuego; deba, una porción del elemento del fuego, una llama. En el
idioma análogo de Letellier (1850) a, quiere decir animal; ab, mamífero; abo, carnívoro; aboj, felino;
aboje, gato; abi, herbívoro; abiv, equino; etcétera. En el de Bonifacio Sotos Ochando (1845), imaba,
quiere decir edificio; imaca, serrallo; imafe, hospital; imafo, lazareto; imari, casa; imaru, quinta;
imedo, poste; imede, pilar; imego, suelo; imela, techo; imogo, ventana; bire, encuadernador; birer,

1
Teóricamente, el número de sistemas de numeración es ilimitado. El más complejo (para uso de las divinidades y
de los ángeles) registraría un número infinito de símbolos, uno para cada número entero; el más simple sólo requiere
dos. Cero se escribe 0, uno 1, dos 10, tres 11, cuatro 100, cinco 101, seis 110, siete 111, ocho 1000... Es invención de
Leibniz, a quien estimularon (parece) los hexagramas enigmáticos del I King.

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encuadernar. (Debo este último censo a un libro impreso en Buenos Aires en 1886: el Curso de
lengua universal, del doctor Pedro Mata.)

Las palabras del idioma analítico de John Wilkins no son torpes símbolos arbitrarios; cada una de
las letras que las integran es significativa, como lo fueron las de la Sagrada Escritura para los
cabalistas. Mauthner observa que los niños podrían aprender ese idioma sin saber que es artificioso;
después en el colegio, descubrirían que es también una clave universal y una enciclopedia secreta.

Ya definido el procedimiento de Wilkins, falta examinar un problema de imposible o difícil

postergación: el valor de la tabla cuadragesimal que es base del idioma. Consideremos la octava
categoría, la de las piedras. Wilkins las divide en comunes (pedernal, cascajo, pizarra), módicas
(mármol, ámbar, coral), preciosas (perla, ópalo), transparentes (amatista, zafiro) e insolubles (hulla,
greda y arsénico). Casi tan alarmante como la octava, es la novena categoría. Ésta nos revela que los
metales pueden ser imperfectos (bermellón, azogue), artificiales (bronce, latón), recrementicios
(limaduras, herrumbre) y naturales (oro, estaño, cobre). La belleza figura en la categoría
décimosexta; es un pez vivíparo, oblongo. Esas ambigüedades, redundancias y deficiencias
recuerdan las que el doctor Franz Kuhn atribuye a cierta enciclopedia china que se titula Emporio
celestial de conocimientos benévolos. En sus remotas páginas está escrito que los animales se
dividen en (a) pertenecientes al Emperador, (b) embalsamados, (c) amaestrados, (d) lechones, (e)
sirenas, (f) fabulosos, (g) perros sueltos, (h) incluidos en esta clasificación, (i) que se agitan como
locos, (j) innumerables, (k) dibujados con un pincel finísimo de pelo de camello, (l) etcétera, (m)
que acaban de romper el jarrón, (n) que de lejos parecen moscas. El Instituto Bibliográfico de
Bruselas también ejerce el caos: ha parcelado el universo en 1000 subdivisiones, de las cuales la 262
corresponde al Papa; la 282, a la Iglesia Católica Romana; la 263, al Día del Señor; la 268, a las
escuelas dominicales; la 298, al mormonismo, y la 294, al brahmanismo, budismo, shintoísmo y
taoísmo. No rehúsa las subdivisiones heterogéneas, verbigracia, la 179: “Crueldad con los animales.
Protección de los animales. El duelo y el suicidio desde el punto de vista de la moral. Vicios y
defectos varios. Virtudes y cualidades varias.”

He registrado las arbitrariedades de Wilkins, del desconocido (o apócrifo) enciclopedista chino y del
Instituto Bibliográfico de Bruselas; notoriamente no hay clasificación del universo que no sea
arbitraria y conjetural. La razón es muy simple: no sabemos qué cosa es el universo. “El mundo
— escribe David Hume— es tal vez el bosquejo rudimentario de algún dios infantil, que lo abandonó
a medio hacer, avergonzado de su ejecución deficiente; es obra de un dios subalterno, de quien los
dioses superiores se burlan; es la confusa producción de una divinidad decrépita y jubilada, que ya
se ha muerto” (Dialogues Concerning Natural Religion, V, 1779). Cabe ir más lejos; cabe sospechar
que no hay universo en el sentido orgánico, unificador, que tiene esa ambiciosa palabra. Si lo hay,
falta conjeturar su propósito; falta conjeturar las palabras, las definiciones, las etimologías, las
sinonimias, del secreto diccionario de Dios.

La imposibilidad de penetrar el esquema divino del universo no puede, sin embargo, disuadirnos de
planear esquemas humanos, aunque nos conste que éstos son provisorios. El idioma analítico de
Wilkins no es el menos admirable de esos esquemas. Los géneros y especies que lo componen son
contradictorios y vagos; el artificio es, sin duda, ingenioso. La palabra salmón no nos dice nada;
zana, la voz correspondiente, define (para el hombre versado en las cuarenta categorías y en los
géneros de esas categorías) un pez escamoso, fluvial, de carne rojiza. (Teóricamente, no es
inconcebible un idioma donde el nombre de cada ser indicara todos los pormenores de su destino,
pasado y venidero.)

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Esperanzas y utopías aparte, acaso lo más lúcido que sobre el lenguaje se ha escrito son estas
palabras de Chesterton: “El hombre sabe que hay en el alma tintes más desconcertantes, más
innumerables y más anónimos que los colores de una selva otoñal… cree, sin embargo, que esos
tintes, en todas sus fusiones y conversiones, son representables con precisión por un mecanismo
arbitrario de gruñidos y de chillidos. Cree que del interior de un bolsista salen realmente ruidos que
significan todos los misterios de la memoria y todas las agonías del anhelo” (G. F. Watts, 1904, pág.
88).

200
 Jorge Luis Borges
Del rigore nella scienza1

… In quell'Impero, l'Arte della Cartografia raggiunse tale Perfezione che la mappa

d'una sola Provincia occupava tutta una Città, e la mappa dell'Impero, tutta una Provin-
cia. Col tempo, codeste Mappe Smisurate non soddisfecero e i Collegi dei Cartografi
eressero una Mappa dell'Impero, che uguagliava in grandezza I'Impero e coincideva
puntualmente con esso. Meno Dedite allo Studio della Cartografia, le Generazioni Suc-
cessive compresero che quella vasta Mappa era Inutile e non senza Empietà la abban-
donarono alle Inclemenze del Sole e degl'Inverni. Nei deserti dell'Ovest rimangono la-
cere Rovine della Mappa, abitate da Animali e Mendichi; in tutto il Paese non è altra re-
liquia delle Discipline Geografiche.

Suàrez Miranda, Viaggi di uomini prudenti, libro quarto, cap. XLV, Lé-
rida, 1658.

Del rigor en la ciencia

… En aquel Imperio, el Arte de la Cartografía logró tal Perfección que el mapa de una
sola Provincia ocupaba toda una Ciudad, y el mapa del Imperio, toda una Provincia.
Con el tiempo, esos Mapas Desmesurados no satisfacieron y los Colegios de Cartógra-
fos levantaron un Mapa del Imperio, que tenía el tamaño del Imperio y coincidía pun-
tualmente con él. Menos Adictas al Estudio de la Cartografía, las Generaciones Siguien-
tes entendieron que ese dilatado Mapa era Inútil y no sin Impiedad lo entregaron a las
Inclemencias del Sol y de los Inviernos. En los desiertos del Oeste perduran despeda-
zadas Ruinas del Mapa, habitadas por Animales y Por Mendigos; en todo el País no hay
otra reliquia de las Disciplinas Geográficas.

Suàrez Miranda, Viajes de varones prudentes, libro cuarto, cap. XLV,

Lérida, 1658.

1 [Tratto da L'artefice, Rizzoli, Milano 1963, trad. Francesco Tentori Montalto, pp. 194-195 (El hacedor,
Emercé Editores S. A., Buenos Aires 1960)].

31-05-2009
201
 TRABAJO PRÁCTICO N° 2
MACROEVOLUCIÓN: DISTINTAS MIRADAS
Sobre el gradualismo, la contingencia y los calamares terrestres

INTRODUCCIÓN GENERAL

La teoría evolutiva puede ser utilizada como un “fin” en sí mismo, pero también como
un “medio”. Es un “fin”, tanto por su enorme poder explicativo como por constituir una de las
piedras fundamentales de la biología, en particular, y de la ciencia en general. Pero al mismo
tiempo, también puede ser un fascinante “medio”. ¿”Medio” para qué? “Medio” para poner en
práctica un ejercicio tan complejo como vital: realizar un análisis crítico del conocimiento
científico.
La teoría evolutiva es obviamente conocimiento. Así, como cualquier conocimiento, se
sustenta en supuestos1. Esto, por cierto, no es negativo. Más aún, es necesario2. Aquellos
supuestos que funcionan como piezas basales para la construcción de ciertos conocimientos se
llaman principios. Poder dar cuenta de ellos o no, constituye un problema que es objeto de un
debate epistemológico entre fundacionistas (quienes creen poder dar cuenta) y no fundacionistas
(quienes consideran que esto no es posible).
Por supuesto que, al tratarse de conocimiento científico, la reflexión adquiere interesantes
particularidades. La importancia de la ciencia no es algo desconocido. La ciencia no es algo
menor, ya que constituye una de las actividades distintivas (y a la vez creadora) del último gran
quiebre que se dio en la historia del hombre: la modernidad.
La particularidad principal y característica del conocimiento científico es su propio
método. Existen profundos y extensos debates al respecto, a partir de la pretensión del
positivismo de reconocer en el método que utiliza la física, al único método aceptable para definir
a la ciencia. Esta concepción, susceptible de ser analizada (y potencialmente aceptada) en
disciplinas como química o biología es sumamente controversial e inadecuada cuando se trata de
otras ciencias que parecen requerir otros métodos, tales como la sociología, la antropología, etc.
¿Dónde radica entonces la fortaleza y la garantía del conocimiento científico? La
legitimación del conocimiento científico, esta dada, no sólo por la confrontación empírica, sino
también por que ha sido consensuado en el ámbito de una comunidad científica. El juicio de los
pares, es la garantía máxima propuesta por aquellos defensores acérrimos de la objetividad
científica, el resguardo para que los supuestos establecidos como prejuicios puedan ser evitados
o, al menos, detectados y aceptados voluntariamente.
¿Cuáles son los contrargumentos frente estas posiciones en apariencia irrebatibles? Una
posible respuesta es que estos prejuicios, frecuentemente, no son del todo entendidos. En el caso
que nos ocupa, no estamos haciendo referencia a prejuicios individuales (traumas infantiles, etc.),
sino especialmente a prejuicios sociales-epocales, a aquellas características culturales generales
1
Estos, cuando no se identifican se transforman en prejuicios.
2
La falta de principios conduce, o bien a una regresión al infinito o bien, a un círculo vicioso. Cualquiera de las dos
situaciones atentan en forma directa contra la construcción de conocimiento.

202
que a su vez definen a una época. Incorporando este contexto cultural, cabe preguntarnos: ¿¡Qué
sentido tendría entonces invocar el juicio de una comunidad científica, como criterio “objetivo”,
cuando a su vez esta comunidad posee los mismos prejuicios que la sociedad en la que se
encuentra inmersa!?
Si uno considera seriamente esta observación, no son menores sus consecuencias. El
contexto cultural no sólo comprometería el marco de interpretación sino que estarían en juego
distintas miradas. Miradas. Los prejuicios nos conforman las miradas, la visión del mundo, o
peor – o mejor, dependiendo desde donde se vea-, constituyen al “mundo”mismo. Este planteo
no cuestiona la importancia del conocimiento científico, sólo se propone reconocer sus límites
identificando y reconsiderando, necesariamente, conceptos tales como “verdad”, “progreso”, etc.

PRIMERA PARTE: Detección de supuestos y prejuicios

1.1. Objetivos:
• Identificar prejuicios en la conformación de un caso de aplicación de pensamiento
evolutivo.
• Ejercitar la fundamentación oral a través de análisis de material audiovisual.
• Realizar un análisis crítico de materiales de divulgación.

1.2. Desarrollo del práctico

El práctico se iniciará con una breve presentación realizada por uno de los docentes. Con
la única consigna de reconocer los prejuicios (previa definición de los mismos), se procederá a la
proyección un fragmento del último capítulo de la serie “Futuro salvaje”. (Duración aproximada:
25 minutos)

Temática general del video presentado:

“Futuro Salvaje responde a la necesidad básica de saber qué pasará en la Tierra cuando
ya no estemos aquí. La serie pretende mostrar cuál será el futuro de nuestro planeta, de
la fauna y flora que lo pueblan y, evidentemente, de la especie humana. Se trata de una
mirada a la posteridad a partir de tres posibles escenarios: dentro de 5, 100 y 200
millones de años. Tres épocas clave en las que se producirán innumerables cambios que
configurarán un mundo completamente distinto al actual. Aumentará la actividad
volcánica, el planeta se calentará y tendrá mucho vapor. Los niveles de oxígeno
aumentarán tanto que los árboles entrarán en combustión espontánea. De estas
transformaciones surgirá un mundo extraordinario poblado por extrañas criaturas y
hábitats inverosímiles. A partir de ahí, se establecerá un nuevo orden mundial en el que
las nuevas especies obtendrán la supremacía. Un escenario que, aunque parezca
ciencia-ficción, es fruto de las hipótesis y predicciones que eminentes científicos de las
teorías evolucionistas han formulado sobre el futuro de la Tierra.” Comentario extraído
de página oficial de Discovery Channel.

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 Posteriormente, se realizará un análisis colectivo de algunos de los supuestos-prejuicios
que se encuentran dicha predicción fílmica, utilizando el siguiente cuestionario como guía:

1.3. Cuestionario guía

a) ¿Cuál es el nivel biológico protagónico?

b) ¿Qué patrones macroevolutivos emergen del video?
c) ¿Qué procesos (macroevolutivos o microevolutivos) se utilizan para explicar la
diversidad?
d) ¿Qué ocurre con el ambiente después de la última extinción en masa?
e) ¿Puede identificar explicaciones de tipo lamarckianas?
f) Como estudiante de la materia evolución, ¿qué opina de este video como material de
divulgación?

SEGUNDA PARTE: Contraposición de dos miradas en torno a la macroevolución

2.1. Marco conceptual para el desarrollo de esta actividad

Las miradas no escapan cuando se ha analizado la evolución. Los biólogos evolutivos
conciben al mundo natural en relación con su historia y como un producto de la misma. En este
sentido, existen interesantes diferencias respecto a los mismos supuestos-prejuicios que se
adoptan y en muchos casos, esas diferencias conllevan a interpretaciones divergentes respecto a
los patrones y a los mecanismos evolutivos que se manifiestan y operan en la historia de la vida.
A modo de presentación didáctica pueden construirse con estos supuestos dos miradas
alternativas susceptibles de ser confrontadas, si bien no resultan completamente excluyentes (ver
figura 1). A cada una de ellas, se la ha caracterizado respecto a elementos relevantes que llevarán
a interpretar la historia de la vida de un modo característico. Entender al mundo como “el mejor
de los mundos posibles” o como “un mero mundo posible” es una diferencia de fondo que
subyace en las concepciones profundas determinantes de cada uno de estos enfoques.
En el siguiente ejercicio Ud. descubrirá que en el primer caso, la mirada macroevolutiva
se identifica con lo que ya ha visto en la materia correspondiente al módulo de Genética de
Poblaciones. Esta mirada es la que ha propuesto gran parte de los “neodarwinistas” del siglo XX.
Sin embargo, cabe aclarar que con fines didácticos se presenta una versión extrema de esta
posición. A esta mirada se le enfrentará otra igualmente extrema, en la cual la macroevolución
posee propiedades y características totalmente diferentes de las nivel microevolutivo. Tomadas
en conjunto, ambas miradas se reúnen en torno a un “darwinismo expandido”, según la propuesta
formulada por S. J. Gould (1983) y discutida en el trabajo práctico pasado. Entender los límites
de una y otra mirada es el objetivo general de este práctico.

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Figura 1. Representación esquemática de las miradas macroevolutivas discutidas en el TP. Se resumen los
principales elementos que las caracterizan y aquellos elementos que comparten.

Mirada A: “El mejor de los mundos posibles”

Bajo esta mirada, llamémosla mirada A, el mundo en el que vivimos es considerado como
“el mejor de los mundos posibles” en términos de su historia evolutiva. Es decir que la diversidad
de la vida actual y sus múltiples formas y relaciones son el resultado de procesos evolutivos que
modelaron durante mucho tiempo el mejor estado posible de la biota en las condiciones
ambientales correspondientes. En cierta medida, esta mirada retoma algunos aspectos generales
de la propuesta original de Darwin y se cristaliza posteriormente de la mano de neodarwinistas
como R. Fischer, T. Dobzhansky, E. Mayr y G. Simpson.
Darwin sostenía que la materia prima de la evolución son las pequeñas diferencias
interindividuales que observamos dentro de las poblaciones. Estas variaciones se fijarían por
selección natural y serían las responsables no sólo de los patrones microevolutivos sino que,
además, producirían los patrones macroevolutivos, debido a que estos pequeños cambios se
acumularían a lo largo de millones de años originando nuevas especies, géneros, familias, etc. En
particular, bajo esta mirada se explica el origen de las especies utilizando ciertos modelos
geográficos de especiación estudiados por Ud. en el módulo correspondiente. En particular, es el
modelo de distribución alopátrica de la especie ancestral el que será inferido con mayor
frecuencia y, en menor medida, los modelos parapátrico y simpátrico.
En líneas generales y de forma característica, esta mirada macroevolutiva supone que el
tempo y el modo de la evolución son de tipo gradual (ver figura 2). El gradualismo está

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íntimamente relacionado con la idea de evolución por selección natural. Si nuevas especies
surgen como un subproducto de la adaptación al ambiente de una especie ancestral, los cambios
deberían ser graduales, ya que un organismo con características muy diferentes a las “óptimas”
no podría tener un gran valor adaptativo (o al menos sería muy poco probable que lo tuviera), y
estos grandes cambios no pasarían a las siguientes generaciones. Por lo tanto, las huellas de
cualquier proceso de especiación estarían dadas por la existencia de formas intermedias o
transicionales entre la especie ancestral y la especie derivada. Para los gradualistas, la
observación de especies que aparecen repentinamente en el registro fósil sin ningún rastro de
formas transicionales se debe a que el mismo es incompleto. Finalmente, todos estos supuestos
aplicados al nivel macroevolutivo conllevan a una reducción de niveles, es decir, abonan la
concepción particular que los patrones y procesos a nivel macroevolutivos son el resultado
directo de los mecanismos que operan a nivel microevolutivo. La macroevolución no constituye,
en consecuencia, un nivel con características emergentes propias.

Figura 2. Para el gradualismo filético, la tasa de cambio

es constante a lo largo del tiempo, inclusive cuando ocurre
un evento de especiación.

Mirada B: “Un mero mundo posible”

En la actualidad muchos biólogos evolutivos “ven” el mundo de forma diferente a la

mirada presentada anteriormente. La llamada mirada B considera que la diversidad de
organismos, sus características y relaciones son el resultado de procesos evolutivos que operaron
en el tiempo, esta vez sujetos a la contingencia de la historia 3. Así, el mundo en el que vivimos no
3
S. J. Gould define a la contingencia en el proceso evolutivo de la siguiente manera:
"Las explicaciones históricas toman la forma de narración: E, el fenómeno a explicar, surgió porque D
ocurrió antes, precedido por C, B y A. Si cualquiera de estos estadios previos no hubiera tenido lugar, o
hubiera sucedido de manera distinta, entonces E no existiría (o estaría presente en una forma
sustancialmente distinta). Así, E tiene sentido y puede ser explicado rigurosamente como resultado del
paso de A a D. Pero ninguna ley de la naturaleza ordenó E; cualquier variante E' que surgiera de un
conjunto alterado de antecedentes habría sido igualmente explicable, aunque absolutamente distinta la
forma y el efecto.
No estoy hablando de aleatoriedad (pues E tenía que surgir, como consecuencia del paso de A a D), sino
del principio fundamental de toda historia: contingencia. Una explicación histórica no descansa sobre
deducciones directas de las leyes de la naturaleza, sino sobre una secuencia impredecible de estados
antecedentes, en la que cualquier cambio importante en cualquier paso de la secuencia habría alterado el
resultado final. Por lo tanto, este estado final depende, o es contingente, de todo lo que ocurrió antes: la
imborrable y determinante rúbrica de la historia."
S.J.Gould (1991). La vida maravillosa. Pp. 354-355.

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es concebido como el mejor mundo posible, sino como uno entre muchos otros mundos posibles.
En este sentido, esta mirada recupera muchas de las propuestas teóricas que han sido formuladas
con posterioridad a la consolidación de la síntesis evolutiva, y por lo tanto, muchas de ellas no
encuentran lugar en dicho marco teórico. Sin embargo, investigadores como Richard Lewontin
(discípulo de T. Dobzhansky), N. Eldredge y S.J. Gould, entre otros, consideran que estos
conceptos deberían ser tenidos en cuenta a la hora de expandir el neodarwinismo, con el fin de
construir un marco teórico robusto basado en una jerarquía de niveles.
Es importante comprender que bajo esta mirada no se niega que la selección natural, la
deriva y el flujo génico sean mecanismos que efectivamente han operado modelando la
variabilidad en el nivel poblacional (ver figura 1). Lo que niegan es que dichos mecanismos
hayan sido los responsables de modelar los patrones de diversidad a nivel macroevolutivo.
Existirían, en su lugar, mecanismos evolutivos con derecho propio que pueden actuar sobre
niveles superiores al de la población, como por ejemplo la simbiogénesis o la selección de
especies. Además, la diversidad de formas observadas actualmente es interpretada como un
resultado de las múltiples restricciones que operan el en proceso evolutivo tanto a nivel del
desarrollo como estructural e histórico. En consecuencia, la macroevolución se hallaría
desacoplada de la microevolución.
En líneas generales y de forma característica, esta mirada macroevolutiva supone que el
tempo y el modo de la evolución son principalmente de tipo discontinuo (ver figura 3). La teoría
de los equilibrios discontinuos (“puntuated equilibria”) fue elaborada por N. Eldredge y S.J.
Gould para explicar por qué el registro fósil no muestra transiciones evolutivas graduales. Estos
investigadores observaron que la mayor parte de los caracteres fenotípicos cambian muy poco
durante largos períodos de tiempo geológico (períodos de equilibrio o estasis), pero cuando
evolucionan, los cambios de un estado al otro ocurren relativamente rápido (períodos en los
cuales la estasis es interrumpida o “puntuada” – “puntuated” en inglés – por el cambio). Bajo este
modelo, el registro fósil refleja un patrón real: las especies aparecen repentinamente, persisten
por ciertos períodos de tiempo y luego se extinguen, dejando escasos signos de formas
intermedias entre el ancestro y el descendiente. En este sentido, un modelo de especiación de tipo
peripátrico podría explicar la rápida aparición de nuevas especies y los cambios aparentemente
direccionales dentro de un clado (las llamadas “tendencias evolutivas”), serían el producto de
fenómenos de especiación y extinción diferencial y no el resultado de la selección natural.

Figura 3. Para el modelo de equilibrios discontinuos,

la tasa de cambio es mínima durante largos períodos
de tiempo (estasis), y es interrumpida por grandes
cambios en tiempos relativamente cortos,
especialmente cuando ocurren eventos
especiogénicos.

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2.2. Objetivos:
• Analizar los supuestos que subyacen a las diferentes concepciones macroevolutivas.
• Comprender la complejidad que reviste el análisis de los patrones biológicos y la
reconstrucción de los mecanismos evolutivos subyacentes.
• Reconocer los principales elementos relacionados con la controversia entre equilibrios
discontinuos vs. gradualismo.

2.3. Desarrollo del práctico:

• Se constituyen grupos de 4-5 personas. A cada grupo se le asigna o bien una Mirada de
tipo A o bien una Mirada de tipo B. A cada uno de los grupos se le da un dibujo de un
animal imaginario4.
• Cada grupo debe dibujar el registro fósil de esa especie en dos momentos previos y dos
momentos posteriores a la existencia de la misma. Los ancestros y descendientes deben
presentarse mediante transformaciones anagenéticas y /o cladogenéticas que reflejen las
“reglas-características” generales de la mirada a la cual pertenecen.
• Cada grupo debe exponer ante sus compañeros las hipótesis propuestas, haciendo una
justificación teórico-práctica de la conformación de los mismos.
• Dos grupos con miradas opuestas deben intercambiarse los dibujos realizados. Cada
grupo debe tratar de reconsiderar y generar hipótesis sobre la filogenia que le fue dada
con su propia mirada (que continúa siendo la asignada originalmente) y exponer esta
nueva interpretación a sus compañeros.
• Cierre general de la actividad haciendo un breve resumen de los elementos centrales que
hayan surgido del ejercicio realizado.

4
Este punto no es menor. La idea es que el individuo realice un análisis crítico y potencie su inventiva, por lo que el
trabajo con organismos ya conocidos podrían dificultar a estos en la medida en que se enfrenten con el conocimiento
previo.

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Bibliografía recomendada para profundizar los temas del módulo:

• J.S. Levinton. La edad de oro de la evolución animal. Investigación y Ciencia. Enero

1993. El autor discute ciertas características de la evolución de los organismos desde la Explosión del
Cámbrico en donde se originaron todos los planes de organización que conocemos actualmente. Propone
que dicha marcha implica una complejización creciente, gradual y tendiente a la adquisición de “mejoras”.
Explica el nivel macroevolutivo a partir de extrapolar evidencias del nivel microevolutivo del cual expone
numerosos ejemplos. Es en este punto en donde queda claro el papel primordial que juega la selección
natural en la adquisición de novedades evolutivas, siendo el azar relegado de esta cuestión.

• S.J. Gould y R. Lewontin. 1985. Los arcos de la catedral de San Marcos y el

paradigma Panglossiano. Mundo Científico 22 (3): 214-223. En esta oportunidad, Gould y
Lewontin se remontan a los arcos de la catedral de San Marcos y a la capilla del King’s College de
Cambridge como claros ejemplos de “adaptación” en arte decorativo. En este marco particular, la palabra
“adaptación” no se presta a confusión, como sucede en biología. Es aquí en donde se ha generalizado un
hábito mental que los autores llaman “programa panglossiano” o programa adaptacionista, según el cual
“las narices han sido hechas para llevar gafas y los pies para ir calzados, por eso tenemos zapatos”. Con
numerosos ejemplos los autores critican el exagerado interés de los biólogos por determinar el valor
adaptativo de las distintas características de los seres vivos, y proponen, a su vez, distintas alternativas.

• S.J. Gould. 1983. El darwinismo y la expansión de la teoría de la evolución.

Interciencia. Número 3 (8): 143-152. De forma muy amena, el autor echa luz sobre el verdadero
significado del término “darwinismo”, cuya esencia yace en su reclamo de que la selección natural es la
principal fuerza directriz de la evolución. Pero, con el paso de los años, esta teoría ha ido modificándose en
tanto nuevos descubrimientos y extensos debates lo exigían. Surge así la Teoría Sintética de la evolución
cuyas críticas nos llevan a replantear las concepciones gradualistas, reduccionistas e hiperadaptaciones del
cambio evolutivo. Se abre entonces, un amplio panorama en donde surgen nuevos modelos para explicarlo,
tomando en cuenta que su complejidad es mucho mayor que la imaginada.

• S.J. Gould. 1994. El Pulgar del Panda. Cap.17. Ed.Crítica. Barcelona. Aquí se exponen
brevemente las razones históricas que llevaron a considerar la aparición de nuevas especies como una lenta
transformación gradual, sólo documentada en parte en el registro fósil. En contrapartida, se explica el
surgimiento de un modelo alternativo, el de los equilibrios discontinuos, en donde la especiación es la
responsable de prácticamente la totalidad del cambio evolutivo. Esta transcurre por breves períodos de
explosión y largos períodos estáticos tal como el registro fósil parece indicar. El papel de la selección
natural queda, en este caso, relegado, mientras que el azar y los procesos estocásticos cobran
preponderancia.

• S.J.Gould. La evolución de la vida en la Tierra. Investigación y Ciencia. Diciembre

1994. En este texto el autor discute los factores que influyeron en la evolución de los organismos haciendo
hincapié en la naturaleza multifactorial de dicho cambio evolutivo. Esto lleva a una complejidad del mundo
la Teoría General de la Evolución puede explicar, e incluso predecir aspectos generales, pero no puede
documentar y comprender la senda real recorrida por la historia de la vida. Para ello hay que acudir a
principios que estén más allá de la Teoría evolutiva.

• Foucault, Michel. Las palabras y las cosas. Pp: 5-10. Comentario por parte del filósofo
francés al pequeño fragmento del cuento de Borges que presenta a través de “cierta Enciclopedia china” los
límites de los esquemas de clasificación y la preconformación de la mirada del hombre. Posteriormente,
Michel Foucault presenta el programa que continuará en su ensayo del análisis de la génesis, características
y límites de nuestra “mirada” como hombres occidentales y modernos.

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 MÓDULO IX

EVOLUCIÓN 
HUMANA
 

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211
 TRABAJOS PRÁCTICOS DE EVOLUCIÓN HUMANA
Ignacio Soto, Ana Liza Tropea & Fernando Ventrice

INTRODUCCIÓN GENERAL
El surgimiento de los homínidos puede ser analizado en el marco de los mecanismos
evolutivos aprendidos y discutidos durante la materia. Muchos aspectos de la evolución del linaje
humano pueden considerarse dentro del marco comprendido por la selección natural ya que todas
las especies, (los homínidos no son excepción) son inherentemente variables y esa variabilidad
afecta la capacidad de los individuos de sobrevivir y reproducirse. Por otro lado, los recursos son
limitados y por lo tanto, existe una competencia entre los individuos por los mismos que resulta en
la supervivencia y reproducción diferencial. Sin embargo, existen otros factores que pueden afectar
la supervivencia y perpetuación de los seres vivos y además, existen otros niveles en los que puede
ocurrir la evolución biológica. Algunos de estos factores constituyen el aspecto contingente de la
evolución. Por ejemplo, cambios climáticos y geológicos a gran escala pueden llevar a la extinción
de poblaciones o especies enteras o crear condiciones competitivas enteramente diferentes. Por otro
lado, el carácter de los cambios evolutivos ocurridos previamente en la historia de un linaje puede
influenciar o limitar el potencial de cambio de la especie. Este factor se conoce como la restricción
filogenética del proceso evolutivo.
A la hora de analizar la evolución humana hay que considerar otro elemento: la
potencialidad evolutiva adquirida con el desarrollo de un cerebro con capacidades no expresadas
previamente por otro organismo en la historia del planeta. Este evento trajo aparejado el
surgimiento de una evolución cultural sin antecedentes, un nuevo nivel evolutivo muy ligado al
desarrollo del lenguaje articulado. Como los mecanismos darwinianos clásicos no son enteramente
aplicables a éste nivel cultural, la cultura humana no puede ser analizada solamente desde la
perspectiva biológica, por regirse por leyes propias, intrínsecamente distintas y cuya complejidad es
irreducible a un plano biológico puro. Podemos pensar a la evolución cultural como un sistema de
cambio más de tipo “lamarckiano” en donde todo lo aprendido en una generación puede ser
transmitido directamente a la siguiente generación por medio de la enseñanza y de la escritura. Los
caracteres adquiridos son transmitidos en la tecnología y la cultura. La evolución lamarckiana es
rápida y acumulativa, es por eso que en tiempos tan pequeños – despreciables para los tiempos
geológicos – nuestra tecnología nos permitió modificar nuestro entorno de manera drástica. La
evolución biológica continúa en Homo sapiens pero lo hace a un ritmo nuevo, al compás de
cambios impuestos (ahora además) por la cultura.
Muchas características que presenta Homo sapiens lo diferencian inclusive de las especies
de primates más cercanas. La naturaleza de estos caracteres puede ser cuantitativa o cualitativa y
abarcan varios niveles de complejidad: desde las diferencias genómicas, pasando por los patrones
de desarrollo hasta llegar al comportamiento, las estrategias reproductivas, la estructura social, el
manejo de la información y la relación de la especie con el resto de la biota. Entender como se
produjeron esos cambios, como influyó el ambiente y cuales fueron las bases genéticas, de
desarrollo o cognitivas que lo permitieron son preguntas fundamentales a responder por la ciencia.
Disciplinas tan disímiles como la genómica comparada, la paleontología y la antropología social
buscan responder partes de este dilema. El desafío último consiste en la conciliación de toda la
información en una explicación completa de la evolución de nuestra especie.
A través de los trabajos prácticos del módulo de Evolución Humana se propone organizar la
discusión alrededor de tres aspectos fundamentales de la evolución de nuestro linaje.
A- ¿Qué nos diferencia de otros primates? El orden Primate incluye una gran diversidad de
familias y especies (Fig. 1). Durante el primer TP se abordará el estudio de ciertos aspectos
característicos de otras especies de primates que constituyen el grupo al cual pertenecemos:
los monos antropoideos. Asimismo, se estudiará la base biológica de nuestro parentesco con

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 los chimpancés, especie viviente más cercanamente emparentada con Homo sapiens. Este
Se propone reflexionar sobre las características que han surgido en ambos linajes luego de la
divergencia.
B- Registro fósil de los homínidos. Recientemente denominados homíninos, este grupo de
primates fósiles bípedos que constituyen nuestro linaje se conoce a través de un nutrido
registro fósil. En el segundo TP de este bloque se propone analizar el patrón que presenta
dicho registro y discutir diferentes interpretaciones posibles. Se hará hincapié en el estudio
de aquellos caracteres que evolucionaron a lo largo del linaje y las particularidades de los
distintos grupos de homíninos, con el objetivo de inferir los procesos evolutivos subyacentes
a dicho patrón.
C- Evolución de Homo sapiens modernos. En el último TP del bloque, se propone estudiar las
evidencias disponibles en la actualidad sobre cuándo y cómo surgen los humanos
anatómicamente modernos, las características anatómicas que permiten reconocerlos, y los
procesos evolutivos que habrían operado modelando dichos rasgos. Se estudiarán en
particular los modelos que existen para explicar el surgimiento del género Homo y de
nuestra especie, analizando las evidencias en las que se basan, las predicciones que elaboran
y, su nivel de correlato con la evidencia de distribución geográfica y temporal.

Figura 1: Árbol filogenético que muestra relaciones de parentesco probables entre distintos grupos de
primates, entre ellos, nuestra especie.

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 SEMINARIO I
ORDEN PRIMATES:
NUESTROS PARIENTES CERCANOS
Por Nicolás Frankel, Ignacio M. Soto & Ana Liza Tropea

Durante este TP se propone reflexionar sobre la base biológica de nuestro parentesco con el
resto de las especies del Orden Primate. Se abordará el estudio de ciertos aspectos característicos
del grupo de especies de primates más cercanamente emparentadas con el humano y que
constituyen el grupo al cual pertenecemos: los monos antropoideos.
Se analizarán luego las características que han surgido en los linajes de chimpancés y
humanos actuales luego de la divergencia desde su ancestro común. Este estudio se abordará a
distintos niveles. En primer lugar, a nivel morfológico a través de los extractos de Fleagle (1999);
en segundo lugar y a nivel molecular, se estudiará la expresión proteica diferencial utilizando parte
del trabajo pionero de King y Wilson (1975); en tercer lugar, la expresión diferencial será estudiada
a partir de los patrones de mRNA evidenciados en el trabajo de Enard et al. (2002). Por último, las
diferencias a nivel de la secuencia misma de ADN serán abordadas con el paper de Clark (2003).

Lea atentamente los siguientes artículos y responda las preguntas que se detallan a continuación:

1. Fleagle, J.G. 1999. Extractos del capítulo 7: “Apes and Humans” en Primate Adaptation and
Evolution. 2da. Ed. Elsevier.

1.1. ¿Cuántas especies de simios africanos viven en la actualidad? Explique el modelo evolutivo
propuesto para este grupo a partir de la figura 7.13.
1.2. ¿Cuáles son las principales similitudes y diferencias entre las especies de hominoideos?
1.3. ¿Por qué considera que resulta dificultoso recuperar una filogenia robusta del grupo de los
monos antropoideos? ¿Qué significa “evolución en mosaico”?

2. King & Wilson. 1975. Evolution at two levels in humans and chimpanzees. Science 188:107-116.

Responda las siguientes preguntas según el contenido de la primera página del artículo (pág. 107):
2.1. En su artículo, King y Wilson mencionan que entre humanos y chimpancés hay diferencias
anatómicas, fisiológicas y comportamentales. ¿Podría especificar algunas diferencias entre
humanos y chimpancés que caen dentro de las categorías de King y Wilson? ¿Estas diferencias
corresponden a cambios ocurridos en el linaje de los humanos o de los chimpancés?
2.2. ¿Cuál es la conclusión general de este fragmento? Preste atención al título del trabajo:
¿Cuáles son los dos niveles de los que se habla?

214
3. Enard, W. et al. 2002. Intra- and interspecific variation in primate gene expression patterns.
Science 296: 340-343.

Para una mejor comprensión del artículo de Enard, W. et al. se incluye una breve
descripción sobre la construcción y uso de los microarreglos. Esta herramienta es adecuada para
encarar estudios a nivel sistémico y es utilizada actualmente para estudiar interrogantes evolutivos.

Los microarreglos

En los últimos años se han secuenciado numerosos genomas completos y se han generado
grandes bases de datos de secuencias transcriptas (cDNAs). Esta valiosa información ha permitido
desarrollar la tecnología de microarray chips.
El microarray de DNA es un vidrio con secuencias de DNA ordenadas en muy poco espacio
físico. Está divido en miles de cuadrados que albergan fragmentos de DNA de secuencia conocida.
Los microarrays de cDNA se fabrican amplificando por PCR fragmentos de 600 a 2400 pares de
bases a partir de clones de libraries de cDNA1. Luego, estos fragmentos doble cadena son
inmovilizados en el vidrio. Los microarrays de oligonucleótidos se fabrican sintetizando in situ
oligonucleótidos de DNA simple cadena de 25 bases o inmovilizando oligonucleótidos de ~70
bases que fueron sintetizados previamente. A diferencia de los microarrays de cDNA, no es
necesario contar con clones de cDNA a partir de los cuales se hace la PCR, simplemente se necesita
tener datos de la secuencia de los genes que se quiere ubicar en el microarray. A partir de esta
secuencia se diseñan los oligonucleótidos a ubicar en el vidrio.
Uno de los usos de los microarrays es el análisis de expresión de genes. La gran cantidad de
genes representados en el arreglo, nos permite hacer estudios a gran escala. La metodología consiste
en extraer RNA en dos condiciones determinadas (o de dos especies distintas) y transformarlo a
cDNA. Al transformar el RNA en cDNA, a este último se le acopla un fluoróforo 2 diferente para
cada una de las dos condiciones. Luego, se juntan en el mismo tubo los cDNAs de las dos
condiciones y se hibridan en el mismo microarray (ver Figura 1) También está la posibilidad de
hibridar los mRNAs de cada condición en un microarray distinto. Luego de lavar el microarray con
alta rigurosidad (para asegurar un pegado específico del cDNA marcado al DNA inmovilizado en el
chip), con un láser se cuantifican las intensidades de los dos fluoróforos para cada gen. Esto nos
indicará cuantitativamente las diferencias en los niveles de expresión de un gen en dos
condiciones o especies distintas.
Los chips son fabricados por empresas (http://www.affymetrix.com;
http://www.appliedbiosystems.com; http://www.agilent.com) o son desarrollados por laboratorios
en universidades o institutos (http://www.microarray.org http://bti.cornell.edu/CGEP/CGEP.html).

1
Una library de cDNA es una colección de secuencias clonadas en plásmido u otro tipo de vector. El cDNA clonado en
el vector se obtuvo a partir de la retrotranscripción del mRNA de un tejido determinado.
2
Un fluoróforo es una molécula que emite fluorescencia en una determinada longitud de onda al ser excitada por luz.

215
 sample 1 sample 2

Fluorophore quantification

Figura 1. Esquema de producción y uso de un microarray de cDNA.

Links de interés:

• http://www.ncbi.nlm.nih.gov/About/primer/microarrays.html
Recuerda las bases moleculares sobre las que se construyeron y pensaron los microarrays.

• http://www.bio.davidson.edu/courses/genomics/chip/chip.html
Una animación que permite ver claramente cómo se hace un experimento con microarrays.

3.1. ¿Por qué cree que se tomaron tres humanos y tres chimpancés para hacer este trabajo?
¿Cuáles son los riesgos de tomar sólo un individuo de orangután?
3.2. a) Los autores no mencionan en ninguna parte del artículo la edad exacta de los primates de
los cuales se obtienen las muestras. Comente los problemas de comparar la expresión de genes
en dos especies con distinta ontogenia y largo de vida.
b) En el trabajo de Enard et al. (2002) se usan muestras de cerebro provenientes únicamente
de primates machos. En un trabajo posterior que tiene similares objetivos al de Enard et al.
(Cáceres et al., 2003) se usan muestras de cerebro de humano y chimpancé de ambos sexos.
¿Cuál de las dos posibilidades le parece la más adecuada?
3.3. Figuras 1 y 2: ¿Qué indican los números sobre las ramas de los árboles? ¿Por qué comparan
los autores la expresión en distintos tejidos? ¿Qué conclusión sacan los autores de los
árboles?
3.4. ¿Para qué cree que se utiliza un grupo externo (orangután o macaco) para analizar
diferencias de expresión entre humano y chimpancé?
3.5. Con un microarray o cualquier otra técnica que mida expresión se pueden detectar
diferencias en los niveles de mRNA entre dos especies. Si el gen X muestra niveles de
mRNA distintos comparando cerebro de chimpancé y humano ¿En qué parte(s) del gen X es
factible que se encuentren diferencias entre las dos especies? ¿Se le ocurre otra hipótesis
para explicar las diferencias en los niveles de mRNA?

216
 3.6. Analice la tabla 1 ¿Qué puede concluir de estos datos?
3.7. En el ya mencionado trabajo de Cáceres et al. (ver pregunta 2), se concluye que de los
genes que muestran distintos niveles de expresión en cerebro entre chimpancé y humano, el
80% presenta niveles más altos en humanos. Si se hace el mismo análisis para corazón e
hígado, se ve que de los genes que muestran distintos niveles de expresión, hay
aproximadamente un 50% que tiene mayor expresión en chimpancé y lógicamente el otro 50
% se encuentra “sobreexpresado” en humano. Entre los genes que se encuentran
“sobreexpresados” en cerebro humano comparado con chimpancé hay muchos que se
agrupan en las siguientes categorías funcionales: 1) mantenimiento y crecimiento celular, 2)
metabolismo de RNA y lípidos y 3) chaperonas.
¿Puede generar alguna hipótesis evolutiva con estos datos?

Bibliografía complementaria de microarrays:

• Duggan, DJ, Bittner, M, Chen, Y, Meltzer, P, Trent, JM. Expression profiling using cDNA
microarrays. Nat Genet. 1999 Jan;21(1 Suppl):10-4.
• Gibson, G and Muse, S. A primer of Genome Science. Pags.195-230. Sinauer Associates,
Inc. 2004.
• Lipshutz RJ, Fodor SP, Gingeras TR, Lockhart DJ. High density synthetic oligonucleotide arrays.
Nat Genet. 1999 Jan;21(1 Suppl):20-4.

4. Clark, A.G. 2003. Inferring Nonneutral Evolution from Human-Chimp-Mouse Orthologous Gene
Trios. Science 302:1960-1963.

4.1. Para una investigación completa sobre la evolución humana a nivel genético no alcanza con conocer
y mapear las diferencias genómicas entre nuestra especie y el resto de las especies de primates. ¿Qué
otra información se necesita?
4.2. ¿Por qué los autores incluyen secuencias de ratón en el análisis? ¿Por qué se trabaja con genes
ortólogos? ¿Cómo se comprueba la relación de ortología entre genes?
4.3. Comente los análisis realizados para poner a prueba la existencia de selección sobre los genes.
4.4. Comente los resultados en relación con las funciones de los genes analizados y los caracteres
involucrados.
4.5. ¿Qué otros análisis completarían los resultados presentados en este trabajo?
4.6. En base a todo lo comentado en el TP, discuta si se puede considerar a los chimpancés como una
especie con caracteres plesiomórficos con respecto a Homo sapiens.

217
Evolution. 2da. Ed. Elsevier.

218
Evolution. 2da. Ed. Elsevier.

219
Evolution. 2da. Ed. Elsevier.

220
Evolution. 2da. Ed. Elsevier.

221
Evolution. 2da. Ed. Elsevier.

222
Fleagle, J.G. 1999. Extractos del capítulo 7: “Apes and Humans” en Primate Adaptation and
Evolution. 2da. Ed. Elsevier.

223
 11 April 1975, Volume 188, Number 4184

evidence concerning the molecular basis

of evolution at the organismal level.
We suggest that evolutionary changes
in anatomy and way of life are more
often based on changes in the mecha-
Evolution at Two Levels in nisms controlling the expression of
genes than on sequence changes in pro-
Humans and Chimpanze es teins. We therefore propose that regula-
tory mutations account for the major
biological differences between humans
Their macromolecules are so alike that regulat4ory and chimpanzees.
mutations may account for their biological differences.
Similarity of Human and
Mary-Claire King and A. C. Wilson Chimpanzee Genes
To compare human and chimpanzee
genes, one compares either homologous
proteins or nucleic acids. At the protein
Soon after the expansion of molecular (Pan troglodytes) and humans (Homo level, one way of measuring the degree
biology in the 1950's, it became evident sapiens). This pair of species is also of genetic similarity of two taxa is to
that by comparing the proteins and unique because of the thoroughness determine the average number of amino
nucleic acids of one species with those with which they have been compared acid differences between homologous
of another, one could hope to obtain at the organismal level-that is, at the polypeptides from each population. The
a quantitative and objective estimate level of anatomy, physiology, behavior, most direct method for determining this
of the "genetic distance" between spe- and ecology. A good opportunity is difference is to compare the amino acid
cies. Until then, there was no common therefore presented for finding out sequences of the homologous proteins.
yardstick for measuring the degree of whether the molecular and organismal A second method is microcomplement
genetic difference among species. The estimates of distance agree. fixation, which provides immunological
characters used to distinguish among The intriguing result, documented in distances linearly correlated with amino
bacterial species, for example, were en- this article, is that all the biochemical acid sequence difference. A third meth-
tirely different from those used for methods agree in showing that the ge- od is electrophoresis, which is useful
distinguishing among mammals. The netic distance between humans and the in analyzing taxa sufficiently closely re-
hope was to use molecular biology to chimpanzee is probably too small to lated that they share many alleles. For
measure the differences in the DNA account for their substantial organismal the human-chimpanzee comparison all
base sequences of various species. This differences. three methods are appropriate, and thus
would be the common yardstick for Indications of such a paradox already many human and chimpanzee proteins
studies of organismal diversity. existed long ago. By 1963, it appeared have now been compared by each
During the past decade, many work- that some of the blood proteins of method. We can therefore estimate the
ers have participated in the develop- humans were virtually identical in degree of genetic similarity between
ment and application of biochemical amino acid sequence with those of humans and chimpanzees by each of
methods for estimating genetic distance. apes such as the chimpanzee or gorilla these techniques.
These methods include the comparison (1). In the intervening years, com- Sequence and immunological com-
of proteins by electrophoretic, immuno- parisons between humans and chimpan- parisons of proteins. During the last
logical, and sequencing techniques, as zees were made with many additional decade, amino acid sequence studies
well as the comparison of nucleic acids proteins and with DNA. These results, have been published on several human
by annealing techniques. The only two reported herein, are consistent with and chimpanzee proteins. As Table 1
species which have been compared by the early results. Moreover, they tell us indicates, the two species seem to have
all of these methods are chimpanzees that the genes of the human and the identical fibrinopeptides (3), cyto-
Dr. King, formerly a graduate student in the
chimpanzee are as similar as those of chromes c (4), and hemoglobin chains
Departments of Genetics and Biochemistry, sibling species of other organisms (2). [alpha (4), beta (4), and gamma (5,
University of California, Berkeley, is now a So, the paradox remains. In order to 6)]. The structural genes for these pro-
research geneticist at the Hooper Foundation and
Department of International Health, University explain how species which have such teins may therefore be identical in hu-
of Califomnia, San Francisco 94143. Dr. Wilson is similar genes can differ so substantially mans and chimpanzees. In other cases,
a professor of biochemistry at the University of
California, Berkeley 94720. in anatomy and way of life, we review for example, myoglobin (7) and the
224
11 APRIL 1975 107
 REPORTS
the duplicates from the same individual con-
Intra- and Interspecific stituted less than 14% of the distances be-
tween individuals. For the liver samples, the

Variation in Primate Gene corresponding value was less than 12%. Be-
cause experimental variation between the tis-

Expression Patterns
sue samples from the same individual was
small, the averages of the pairwise distances
measured between the duplicates for each
Wolfgang Enard,1* Philipp Khaitovich,1* Joachim Klose,2 tissue sample were used to estimate a tree
Sebastian Zöllner,1 Florian Heissig,1 Patrick Giavalisco,3 depicting the overall differences in gene ex-
Kay Nieselt-Struwe,4 Elaine Muchmore,5,6 Ajit Varki,5 pression measured between individuals. The
Rivka Ravid,7 Gaby M. Doxiadis,8 Ronald E. Bontrop,8 results (Fig. 1A) show that the variation in
gene expression between individuals within
Svante Pääbo1† the species is substantial, relative to the dif-
ferences between humans and chimpanzee.
Although humans and their closest evolutionary relatives, the chimpanzees, are For example, one human brain sample differs
98.7% identical in their genomic DNA sequences, they differ in many mor- more from the other human samples than the
phological, behavioral, and cognitive aspects. The underlying genetic basis of latter differ from the chimpanzee samples.
many of these differences may be altered gene expression. We have compared However, for both the brain and liver sam-
the transcriptome in blood leukocytes, liver, and brain of humans, chimpanzees, ples, the humans, as well as the chimpanzees,
orangutans, and macaques using microarrays, as well as protein expression fall into two mutually exclusive groups when
patterns of humans and chimpanzees using two-dimensional gel electrophore- their gene expression patterns are related to
sis. We also studied three mouse species that are approximately as related to that seen in the orangutan, which is evolu-
each other as are humans, chimpanzees, and orangutans. We identified species- tionarily further removed from humans and
specific gene expression patterns indicating that changes in protein and gene chimpanzees than these are from each other.
expression have been particularly pronounced in the human brain. When statistically tested by a bootstrap ap-
proach, this observation is supported in both
Striking differences in morphology and cog- rhesus macaques (Macaca mulatta). For liver and brain (7 ). Thus, a number of gene
nitive abilities exist between humans and comparative purposes, we performed similar expression differences between humans and
their closest evolutionary relatives, the chim- studies in rodent species that have diverged chimpanzees are shared among all individu-
panzees. At least some of these differences from each other approximately as much as als analyzed from each species. The amount
can be assumed to form the basis for the humans and the great apes. of gene expression differences shared among
complex and rapid cultural evolution and de- First, we compared mRNA levels in brain all humans is larger than those shared among
mographic explosions that have characterized and liver of humans, chimpanzees, and a all chimpanzees. One likely factor contribut-
recent human evolution (1). In addition, hu- orangutan using Affymetrix U95A arrays (5), ing to this is that oligonucleotides comple-
mans and chimpanzees differ in several other which contain oligonucleotides that examine mentary to human cDNAs are used to assay
traits that are of medical interest, such as approximately 12,000 human genes. From RNA levels not only in humans but also in
susceptibility to AIDS, epithelial neoplasms, the brain, gray matter from the left prefrontal chimpanzees and orangutans. Thus, nucleo-
malaria, and Alzheimer’s disease (2, 3). Al- lobe (Brodmann area 9) was removed at au- tide sequence differences between the last-
though it was pointed out 25 years ago (4) topsies from three adult male humans, three named species and humans can be expected
that many of these differences may be due to adult male chimpanzees, and one adult male to reduce the apparent expression levels mea-
quantitative differences in gene expression orangutan. For brain and liver, two indepen- sured in the apes. Such differences will be
rather than structural changes in gene prod- dent isolations of RNA from adjacent tissue assigned to the human lineage. However, the
ucts, nothing is known about how gene ex- samples were performed for each individual apparent acceleration on the human lineage is
pression profiles differ between humans and and analyzed independently (5). larger in the brain (3.8-fold) than in the liver
chimpanzees. In order to take a first step All possible pairwise comparisons among (1.7-fold), raising the possibility that gene
toward understanding the evolution of the the six human, six chimpanzee, and two or- expression patterns may have changed more
mammalian transcriptome and proteome, we angutan samples were made for each tissue, in the brain than in the liver during recent
studied mRNA expression levels, as well as and the differences in apparent expression human evolution.
protein expression patterns, in different tis- levels were used to calculate an overall dis- To investigate the latter possibility, we
sues of humans, chimpanzees (Pan troglo- tance summarized over all genes (6). For the performed a second set of experiments using
dytes), orangutans (Pongo pygmaeus), and brain samples, the distances measured among membrane-based cDNA arrays carrying

1
Max-Planck-Institute for Evolutionary Anthropology, Table 1. Brain protein pattern differences between humans and chimpanzees as analyzed by 2D gel
Inselstrasse 22, D-04103 Leipzig, Germany. 2Institut electrophoresis (16). Differences between humans and chimpanzees were scored if confirmed in three
fuer Humangenetik Charité, D-13353 Berlin, Germa- individual human-chimpanzee pairs and were analyzed in the same way as in a larger mouse study
ny. 3Max-Planck-Institute for Molecular Genetics, comparing M. musculus and M. spretus (23). Qualitative differences represent changes in electrophoretic
D-14195 Berlin, Germany. 4Max-Planck-Institute of mobility of spots, which likely result from amino acid substitutions, whereas quantitative differences
Biophysical Chemistry, D-37077 Göttingen, Germany. reflect changes in the amount of protein.
5
University of California San Diego, La Jolla, CA
92093, USA. 6VA Medical Center, San Diego, La Jolla,
Differences
CA 92093, USA. 7The Netherlands Brain Bank, Am-
sterdam, the Netherlands. 8Biomedical Primate Re- Comparison Analyzed spots
search Centre, Rijswijk, the Netherlands. Qualitative Quantitative
*These authors contributed equally to this work. Human– chimpanzee 538 41 (7.6%) 169 (31.4%)
†To whom correspondence should be addressed. E- M. musculus–M. spretus 8767 668 (7.6%) 656 (7.5%)
mail: paabo@eva.mpg.de
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340 12 APRIL 2002 VOL 296 SCIENCE www.sciencemag.org
 REPORTS
21,504 DNA sequences of an average length humans. This is due to a 5.5-fold acceleration frontal cortex. As in the primates, the gene
of ⬃1,000 bp, amplified from 17,997 human of the rate of change in gene expression expression patterns within species show great
genes of the Unigene set (8). When such long levels on the lineage leading to humans. variation (Fig. 1B), as recently reported even
target sequences are used, the average nucle- Thus, the results show that the rate of evolu- for inbred mice (15). However, when the
otide sequence difference of around 0.8% tionary change of gene expression levels in more distantly related M. caroli is taken into
between human and chimpanzee cDNAs (9) the brain is accelerated in the human evolu- account, it is clear that all M. musculus and
is not expected to influence the results signif- tionary lineage relative to the chimpanzee, M. spretus individuals share gene expression
icantly. For these experiments, brain neocor- whereas no such acceleration is evident in patterns that separate them from the other
tex samples from the autopsies of seven hu- liver or blood. It should be noted, however, species, as is the case for humans and chim-
mans, four chimpanzees and two macaques that the extent of the acceleration is highly panzees. When these species-specific differ-
were used, as well as liver samples from six dependent on the metric used. ences are compared, it is found that the
humans, five chimpanzees, and four ma- To gauge whether the observations made change on the line to M. musculus is 2.1-fold
caques. In addition, blood samples were col- among the primate species are typical of and 2.3-fold that in brain and liver, respec-
lected from 10 humans, 10 chimpanzees, and mammals, we investigated the three mouse tively. Thus, as in the case of the primate
10 rhesus macaques. To allow the same filter species, Mus spretus, M. caroli, and M. mus- analyses, the species for which the oligonu-
arrays to be used throughout the experiments, culus, among which the former two species cleotide array was designed shows an appar-
equal amounts of RNA from a given species differ from M. musculus at silent sites, i.e., at ent acceleration, which is likely to be due to
and tissue were pooled, labeled, and hybrid- sites that do not change the encoded amino nucleotide sequence differences between the
ized to the cDNA arrays (10). acids, by approximately 2.5% and 4.5%, re- species analyzed. However, in the rodents,
The relative rates of evolutionary change spectively (12). Thus, their extent of diver- this acceleration is of similar magnitude in
in the transcriptomes of the three tissues were gence from M. musculus is in the same order brain and liver, and as expected from the
estimated (11), using the macaque as an out- of magnitude as that of chimpanzees (1.08%) slightly higher genomic divergence, it is
group (Fig. 2). For both blood leukocytes and and orangutans (2.98%), respectively, from slightly higher than that seen in primate liver.
liver, the human expression patterns are more humans (13, 14 ). Affymetrix arrays carrying Thus, these results show that gene expression
similar to those of the chimpanzees than to oligonucleotides specific for 12,000 M. mus- differences are substantial between closely
those of the macaques, reflecting the evolu- culus genes (5) were used to analyze samples related mammalian species and supports the
tionary relationships of the species. Further- from the frontal part of the brains and livers notion that changes in gene expression levels
more, the extent of change on the lineages from three individuals of M. musculus, three in the brain may have been especially pro-
leading to the chimpanzees and the humans individuals of M. spretus, and one individual
are equal in leukocytes and 1.3-fold different of M. caroli. To make the experiments as
in liver. In stark contrast, the expression pat- comparable as possible to the analysis of the
tern in the chimpanzee brain cortex is more humans and apes, outbred mice were used,
similar to that of the macaques than to that of and only gray matter was sampled from the

Fig. 2. Distance trees representing the relative

extent of expression changes among three pri-
Fig. 1. Distance trees representing the relative extent of expression changes in brain and liver mate species and three tissues as assayed by
among (A) three primate and (B) three mouse species: MUS., M. musculus; SPR., M. spretus; and the cDNA arrays (11). Numbers refer to the
CAR, M. caroli (6). Numbers refer to the ratio between the changes common to humans and ratio between the changes common to humans
chimpanzees, and M. musculus and M. spretus, respectively. and chimpanzees.
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 REPORTS

Fig. 3. Two-dimensional gel electrophoresis of proteins from the cyto- changes. For each type of variation, a few examples are indicated. From
solic fraction of human (A) and chimpanzee (B) cortex frontalis. From the identification by mass spectrometry in both humans and chimpanzees,
total pattern, comprising about 8500 protein spots, a representative these proteins spots are 1, aldose reductase (gi576365); 4, carbonic
section consisting of about 200 spots is shown. Protein patterns from dehydratase (gi4502517); 5, electron transfer flavoprotein
human and chimpanzee were compared, and changes between homolo- (gi2781202); 6, hypothetical protein DKFZp564D1378 (gi14149777);
gous spots found in all three human-chimpanzee pairs were scored. Three 10, ␦-aminolevulinate dehydratase (gi2118316); 11, CGI-105 protein
different types of variations were registered: (i) variations in electro- (gi11431155); 13, hypothetical protein XP_047816 (gi14743583); 14,
phoretic mobility of spots (7), most likely due to mutations affecting malate dehydrogenase 2 (gi5174541); 15, MAWD-binding protein
the structure of proteins (e.g., amino acid substitutions); (ii) variations in (gi16307296); 16, uncharacterized hypothalamus protein HCDASE
spot intensity (1 or 2) reflecting alterations in protein amount, possibly (gi8923864); 30, purine nucleoside phosphorylase (gi4557801); 31,
due to mutations in regulatory genes; and (iii) presence or absence purine nucleoside phosphorylase (gi4557801); and 35, aldehyde reduc-
variations (⫹ or ⫺), which may also result from quantitative tase (gi1633300).

nounced during recent human evolution. For the two rodents, the relative amounts of References and Notes
Differences in mRNA levels do not nec- quantitative protein differences are similar 1. G. Klein, The Human Career: Human Biological and
essarily translate into differences in protein to the qualitative differences. In contrast, Cultural Origins ( The Univ. of Chicago Press, Chicago,
1989).
levels. Therefore, we investigated whether quantitative differences are approximately 2. P. Gagneux, A. Varki, Mol. Phylogenet. Evol. 18, 2
quantitative changes not only in RNA lev- 6 times as common as qualitative differenc- (2001).
els but also in protein levels are especially es when chimpanzee and human brains are 3. A. Varki, Genome Res. 10, 1065 (2000).
4. M. C. King, A. C. Wilson, Science 188, 107 (1975).
pronounced in the brain during recent hu- compared. Thus, the human brain has prob- 5. All apes used in this study died of natural causes. In
man evolution. We studied protein patterns ably experienced more evolutionary chang- all cases, postmortem times were shorter than 6
in the brains of humans and chimpanzees, es in gene expression both at the mRNA hours, and only minimal RNA degradation was seen
by agarose electrophoresis. Preparation of the sam-
as well as in M. musculus and M. spretus to and protein levels than the two mouse spe- ples for the Affymetrix arrays, hybridization, and
put the primate differences into perspective cies. In this regard, a recent comparison of scanning were performed as described (18). Nine of
(16 ). In each case, the tissue samples were human and great ape blood plasma proteins 10 genes that differed at least twofold between
human and chimpanzee brains could be verified by a
removed from sites adjacent to the ones (17 ) found only one human-specific differ- Northern analysis. Details of experimental proce-
used in the first set of mRNA analyses from ence. This is in contrast to the many differ- dures are available on Science Online at www.
the same individuals. Soluble proteins were ences found here for soluble brain proteins sciencemag.org/cgi/content/full/296/5566/340/DC1
isolated by differential centrifugation, sep- and supports a more rapid rate of evolution and on http://email.eva.mpg.de/⬃khaitovi/
supplement1.html.
arated on two-dimensional (2D) polyacryl- of protein expression levels in the brain. 6. Affymetrix array results were carried out with Mi-
amide gels, and visualized by silver stain- Our results show that that large numbers croarray Suite, version 4.0 (Affymetrix) by using de-
ing (Fig. 3). Two types of differences were of quantitative changes in gene expression fault settings. All arrays were normalized to the same
target intensity using all probe sets. The difference in
scored: (i) shifts in the migration positions can be detected between closely related mam- scaling factor was less than threefold among all
of proteins, which represent a shift in size mals. They furthermore suggest that such arrays. In order to build distance trees, pairwise dis-
or charge of the protein, i.e., covalent dif- changes have been particularly pronounced tances between samples were calculated as the sum
of the base-two logarithms of the absolute values of
ference that in most cases are changes in during recent evolution of the human brain. the “fold change” for all 12,000 genes represented on
amino acid sequence; (ii) differences in The underlying reasons for such expression a chip. When “absent calls” were assigned to both
quantity of proteins without a shift in mi- differences are likely to be manifold, for ex- samples in a comparison, and when the difference
call for the gene was “no change,” the fold change
gration position which represent differenc- ample, duplications and deletions of genes, value was set to zero. The resulting distance matrix
es in amounts of protein expressed in the promotor changes, changes in levels of tran- was used to build neighbor joining trees (19) as
tissue. The relative amounts of qualitative scription factors, and changes in cellular implemented in the PHYLIP package (20). The full
data set is available at http://email.eva.mpg.de/
protein differences observed between hu- composition of tissues. A challenge for the ⬃khaitovi/supplement1.html
mans and chimpanzees and between M. future is to investigate the relative contribu- 7. The reliability of the distance trees branching pattern
musculus and M. spretus, respectively, are tions of these factors to the expression differ- was estimated by 1000 bootstrap samples of the
similar ( Table 1), as expected from the ences observed. A further challenge is to 12,000 genes. The bootstrap values for the species
were ⬎99.9% in all cases except for the chimpanzee
similar extent of genomic DNA sequence clarify how many of the differences have brain branch, where in the remaining 16% of cases,
differences between the two species pairs. functional consequences. the orangutan fell among the chimpanzees. There
227
342 12 APRIL 2002 VOL 296 SCIENCE www.sciencemag.org
 REPORTS
was 100% bootstrap support for the separation of tingen, and K. Krohn and Petra Süptitz from the Inter- ulating discussions. We also thank the Bundesministe-
the mouse species in both tissues. disziplinäres Zentrum für Klinische Forschung (IZKF), rium für Bildung und Forschung, the Saxonium Ministry
8. M. S. Boguski, G. D. Schuler, Nature Genet. 10, 369 Leipzig, for the help with microarray experiments; T. for Science, and the Max Planck Gesellschaft for financial
(1995). Kitano for analyzing the mouse divergence; D. Kuhl for support.
9. I. Hellmann, unpublished data. initial advice in the project; and many people at Max
10. All RNA pools were hybridized 4 to 6 times to the Planck Institute for Evolutionary Anthropology for stim- 14 December 2001; accepted 27 February 2002
same set of filters in order to estimate interexperi-
mental errors and to minimize their effects
through the combined analysis of several experi-
ments. Signals that were at least 5 times above
background and not influenced to more than 25%
by neighboring spots were further analyzed. A gene
A MADS-Box Gene Necessary
was regarded as differently expressed if it fulfilled
two criteria: (i) The difference in signal between
two species was at least two-fold; and (ii) the
for Fruit Ripening at the
signal between the two species was significantly
different as determined by a paired t test. Sixteen
differently expressed genes were analyzed by
Tomato Ripening-Inhibitor (Rin)
Northern blots, and 1 out of 12 that were detected
by the Northern analyses yielded results contra-
dictory to the arrays, whereas the remaining 11
Locus
showed expression patterns that were both quali-
tatively and quantitatively similar in all three spe-
Julia Vrebalov,1,2 Diane Ruezinsky,2
cies to that detected by the arrays. Details of Veeraragavan Padmanabhan,2 Ruth White,1,2 Diana Medrano,1,2
experimental procedures are available on Science
Online at www.sciencemag.org/cgi/content/full/
Rachel Drake,3 Wolfgang Schuch,3 Jim Giovannoni1*
296/5566/340/DC1and on http://email.eva.
mpg.de/⬃khaitovi/supplement1.html.
11. The distance between two expression profiles of two Tomato plants harboring the ripening-inhibitor (rin) mutation yield fruits that fail
species in a given tissue was determined by summing to ripen. Additionally, rin plants display enlarged sepals and loss of inflorescence
up the absolute ratios of the included genes given by determinacy. Positional cloning of the rin locus revealed two tandem MADS-box

冘 冘  genes (LeMADS-RIN and LeMADS-MC), whose expression patterns suggested roles

n
x ji
the formula: log2
x ik
, where n is the number in fruit ripening and sepal development, respectively. The rin mutation alters
i⫽1
expression of both genes. Gene repression and mutant complementation demon-
of included genes, and is the normalized intensity of strate that LeMADS-RIN regulates ripening, whereas LeMADS-MC affects sepal
gene i as measured in species j. In order to avoid the
contribution of genomic differences, only those differ- development and inflorescence determinacy. LeMADS-RIN demonstrates an
ently expressed genes were considered that did not agriculturally important function of plant MADS-box genes and provides mo-
show the same expression difference in two or more lecular insight into nonhormonal (developmental) regulation of ripening.
tissues. The resulting distance matrix was used to build
neighbor joining trees (19) as implemented in the
PHYLIP package (20). The data are available at http:// The maturation and ripening of fleshy fruits respiration or increased ethylene for matura-
email.eva.mpg.de/⬃khaitovi/supplement1.html is a developmental process unique to plants tion. Molecular ripening research has focused
12. We retrieved nonmitochondrial nucleotide sequences and affects the quality and nutritional content primarily on ethylene, but little is known of
from M. spretus (10 sequences) and M. caroli (11
sequences) from GenBank and compared them with of a significant portion of the human diet. control before ethylene induction, nor of
the corresponding M. musculus sequence. The aver- Although specific fruit-ripening characteris- common regulatory mechanisms shared by
age number of substitutions at silent sites was esti- tics vary among species, ripening can be gen- climacteric and nonclimacteric species (3).
mated to be 0.025 (⫾ 0.006) for M. spretus and
0.045 (⫾ 0.008) for M. caroli.
erally described as the coordinated manifes- The tomato is a model for analysis of
13. F. C. Chen, W. H. Li, Am. J. Hum. Genet. 68, 444 (2001). tation of changes in color, texture, flavor, ripening due originally to its significance as
14. A. Fujiyama et al., Science 295, 131 (2002). aroma, and nutritional characteristics that a food source and diverse germplasm, and
15. C. C. Pritchard, L. Hsu, J. Delrow, P. S. Nelson, Proc. render fruit attractive to organisms receiving more recently, the availability of molecular
Natl. Acad. Sci. U.S.A. 98, 13266 (2001).
16. Fractionation, 2D gel electrophoresis, and matrix-
sustenance in exchange for assisting in seed tools (4 ) and efficient transformation (5). A
assisted laser desorption time-of-flight (MALDI- dispersal (1, 2). number of tomato-ripening mutants have
TOF) mass spectrometry were done as described in Fruit species are classically defined as one been useful for research and breeding (3).
(21–23).
17. P. Gagneux et al., Am. J. Phys. Anthropol. 115, 99
of two ripening types, climacteric and non- Especially interesting is the recessive rip-
(2001). climacteric, where the former display a burst ening-inhibitor (rin) mutation that inhibits
18. L. Wodicka, H. Dong, M. Mittmann, M. H. Ho, D. J. in respiration at the onset of ripening, in all measured ripening phenomena, includ-
Lockhart, Nature Biotechnol. 15, 1359 (1997). contrast to the latter. Climacteric fruit typi- ing the respiratory climacteric and associ-
19. N. Saitou, M. Nei, Mol. Biol. Evol. 4, 406 (1987).
20. J. Felsenstein, PHYLIP (Phylogeny Inference Package,
cally increase biosynthesis of the gaseous ated ethylene evolution, pro-vitamin A
version 3.5c; Department of Genetics, Univ. of Wash- hormone ethylene, which is required for the carotenoid accumulation, softening, and
ington, Seattle (1993). ripening of fruit such as tomatos, bananas, production of flavor compounds (6 ). The
㛬㛬㛬㛬
21. J. Klose, Methods Mol. Biol. 112, 67 (1999). apples, pears, and most stone fruit. Noncli- rin mutant exhibits ethylene sensitivity, in-
㛬㛬㛬㛬
22. , Methods Mol. Biol. 112, 147 (1999).
23. et al., Nature Genet. 30, 385 (2002); pub- macteric fruit, including strawberries, grapes, cluding the seedling triple response (7 ),
lished online 25 March 2000 (10.1038/ng 861). and citrus fruits, do not require climacteric floral abscission, and petal and leaf senes-
24. We thank C. Allen and T. Insel of the Yerkes Primate cence. Nevertheless, rin fruit do not ripen
Center, Atlanta, for chimpanzee tissues; T. Arendt and U.
Überham of the Paul Flechsig Institute, Leipzig, for hu- 1
U.S. Department of Agriculture–Agricultural Re- in response to exogenous ethylene, yet they
man and mouse tissue dissections; E. Kuhn at the Bio- search Service (USDA-ARS) Plant, Soil and Nutrition display induction of at least some ethylene-
medical Primate Research Centre, Rijswijk, for autopsies; Lab and Boyce Thompson Institute for Plant Research, responsive genes, indicating retention of
H. Zischler and K. Mätz-Rensing from the German Pri- Cornell University, Ithaca, NY 14853, USA. 2Texas
mate Center, Göttingen, for macaque samples; C. Wit-
fruit ethylene sensitivity (8). We interpret
A&M University, Department of Horticultural Scienc-
tekind and U. Gütz from the University of Leipzig for liver es, College Station, TX 77843, USA. 3Zeneca Plant
these results to mean that the RIN gene en-
resections; E. Edel from the University of Leipzig for Sciences (Syngenta), Jeallots Hill Research Station, codes a genetic regulatory component neces-
human blood samples; F. Bonhomme and A. Orth of the Bracknell, Berkshire RG12 6EY, UK. sary to trigger climacteric respiration and rip-
Université Montpellier II for the mouse tissues; J. Retief
at Affymetrix for help and support; K. Chowdhury from *To whom correspondence should be addressed. E- ening-related ethylene biosynthesis in addi-
the Max-Planck-Institute of Biophysical Chemistry, Göt- mail: jjg33@cornell.edu tion to requisite factors whose regulation is
228
www.sciencemag.org SCIENCE VOL 296 12 APRIL 2002 343
 REPORTS
and LED 8 (541 observed, 456 expected, P ⬍ 3. D. Milioni, P. E. Sado, N. J. Stacey, K. Roberts, M. C. tory (www.plantsci.cam.ac.uk/Haseloff/Home.html).
McCann, Plant Cell 14, 2813 (2002). The lines were obtained through the Arabidopsis In-
0.0006)—providing evidence in plants for a link formation Resource (www.arabidopsis.org/).
4. P. J. Roy, J. M. Stuart, J. Lund, S. K. Kim, Nature 418, 975
between genome organization and gene regulation. (2002). 22. Y. Lin, J. Schiefelbein, Development 128, 3697 (2001).
Together these data provide an organ ex- 5. H. Jasper et al., Dev. Cell 3, 511 (2002). 23. M. M. Lee, J. Schiefelbein, Cell 99, 473 (1999).
pression map, revealing putative localized hor- 6. P. N. Benfey, J. W. Schiefelbein, Trends Genet. 10, 84 24. E. Truernit, N. Sauer, Planta 196, 564 (1995).
(1994). 25. We thank J. Malamy for valuable ideas on the proto-
mone-response domains and a complex pattern 7. Materials and methods are available as supporting plasting technique; H. Petri, K. Gordon, and J. Hirst for
of regulatory genes that could mediate primary material on Science Online. assistance in cell sorting; H. Dressman and the Duke
developmental cues. These data should help 8. J. Sheen, Plant Physiol. 127, 1466 (2001). Microarray Core Facility for assistance with microar-
9. J. Quackenbush, Nature Rev. Genet. 2, 418 (2001). rays; A. Pekka Mähönen and Y. Helariutta for use of
identify candidate genes involved in pattern 10. The program Cluster was used in the analysis and down- the pWOL::GFP line and M. Cilia and D. Jackson for
formation and cell specificity in the root, which loaded from http://rana.lbl.gov/EisenSoftware.htm. the pSUC2::GFP line, both before publication; M.
is a model for organogenesis. The expression 11. M. B. Eisen, P. T. Spellman, P. O. Brown, D. Botstein, Levesque for valuable discussions; and G. Sena and T.
Proc. Natl. Acad. Sci. U.S.A. 95, 14863 (1998). Nawy for photos. This work was supported by NSF
map will also facilitate both computational and 12. K. Birnbaum et al., unpublished data. grants MCB-020975 (P.N.B. and D.E.S.), DBI-9813360
experimental methods aimed at decoding regu- 13. T. Berleth, J. Mattsson, Curr. Opin. Plant Biol. 3, 406 (2000). (D.W.G.), DBI-0211857 (D.W.G.), and a Small Grant
latory mechanisms in the root. Thus, these re- 14. U. Wittstock, B. A. Halkier, Trends Plant Sci. 7, 263 (2002). for Exploratory Research (P.N.B. and D.E.S.). The NIH
sults can now be used to explore how the 15. L. L. Murdock, R. E. Shade, J. Agric. Food Chem. 50, supported K.B. with a postdoctoral fellowship grant
6605 (2002). (5 F32 GM20716-03).
hundreds of different expression patterns they 16. B. A. Cohen, R. D. Mitra, J. D. Hughes, G. M. Church,
reveal are established and interpreted at the Nature Genet. 26, 183 (2000). Supporting Online Material
17. H. Caron et al., Science 291, 1289 (2001). www.sciencemag.org/cgi/content/full/302/5652/1956/
cellular level to generate a complex organ. DC1
18. A. P. Mahonen et al., Genes Dev. 14, 2938 (2000).
19. M. Bonke, S. Thitamadee, A. P. Mahonen, M. T. Materials and Methods

Downloaded from www.sciencemag.org on August 2, 2010

References and Notes Hauser, Y. Helariutta, Nature, in press. Figs. S1 to S3
1. N. M. Kerk, T. Ceserani, S. L. Tausta, I. M. Sussex, T. M. 20. J. W. Wysocka-Diller, Y. Helariutta, H. Fukaki, J. E. Tables S1 to S4
Nelson, Plant Physiol. 132, 27 (2003). Malamy, P. N. Benfey, Development 127, 595 (2000).
2. T. Asano et al., Plant J. 32, 401 (2002). 21. The plant line was generated by the Haseloff labora- 4 August 2003; accepted 15 October 2003

Inferring Nonneutral Evolution average nucleotide divergence of just 1.2%

(3–5). The role of protein divergence in caus-

from Human-Chimp-Mouse ing morphological, physiological, and behav-

ioral differences between these two species,
however, remains unknown.
Orthologous Gene Trios Here we apply evolutionary tests to iden-
tify genes and pathways from a new collec-
Andrew G. Clark,1 Stephen Glanowski,3 Rasmus Nielsen,2 tion of more than 200,000 chimpanzee exonic
Paul D. Thomas,4 Anish Kejariwal,4 Melissa A. Todd,2 sequences that show patterns of divergence
David M. Tanenbaum,5 Daniel Civello,6 Fu Lu,5 Brian Murphy,3 consistent with natural selection along the
human and chimpanzee lineages.
Steve Ferriera,3 Gary Wang,3 Xianqgun Zheng,5 To construct the human-chimp-mouse
Thomas J. White,6 John J. Sninsky,6 Mark D. Adams,5* alignments, we sequenced PCR amplifica-
Michele Cargill6† tions using primers designed to essentially all
human exons from one male chimpanzee,
Even though human and chimpanzee gene sequences are nearly 99% identical, se- resulting in more than 20,000 human-chimp
quence comparisons can nevertheless be highly informative in identifying biologically gene alignments spanning 18.5 Mb (6 – 8). To
important changes that have occurred since our ancestral lineages diverged. We an- identify changes that are specific to the di-
alyzed alignments of 7645 chimpanzee gene sequences to their human and mouse vergence in the human lineage, we compared
orthologs. These three-species sequence alignments allowed us to identify genes the human-chimp aligned genes to their
undergoing natural selection along the human and chimp lineage by fitting models mouse ortholog. Inference of orthology in-
that include parameters specifying rates of synonymous and nonsynonymous volved a combination of reciprocal best
nucleotide substitution. This evolutionary approach revealed an informative set of matches and syntenic evidence between hu-
genes with significantly different patterns of substitution on the human lineage man and mouse gene annotations (9, 10).
compared with the chimpanzee and mouse lineages. Partitions of genes into in- This genome-wide set of orthologs under-
ferred biological classes identified accelerated evolution in several functional class- went a series of filtering steps to remove
es, including olfaction and nuclear transport. In addition to suggesting adaptive ambiguities, orthologs with little sequence
physiological differences between chimps and humans, human-accelerated genes data, and genes with suspect annotation (6).
are significantly more likely to underlie major known Mendelian disorders. The filtered ortholog set was compared to

Although the human genome project will al- gence caused by random drift and divergence 1
Molecular Biology and Genetics, 2Biological Statistics
low us to compare our genome to that of driven by natural selection. Early observa- and Computational Biology, Cornell University, Ithaca,
NY 14853, USA. 3Applied Biosystems, 45 West Gude
other primates and discover features that are tions of unexpectedly low levels of protein Drive, Rockville, MD 20850, USA. 4Protein Informatics,
uniquely human, there is no guarantee that divergence between humans and chimpan- Celera Genomics, 850 Lincoln Centre Drive, Foster City,
such features are responsible for any of our zees led to the hypothesis that most of the CA 94404, USA. 5Celera Genomics, 45 West Gude Drive,
unique biological attributes. To identify evolutionary changes must have occurred at Rockville, MD 20850, USA. 6Celera Diagnostics, 1401
Harbor Bay Parkway, Alameda, CA 94502, USA.
genes and biological processes that have been the level of gene regulation (1). Recently,
most altered by our recent evolutionary di- much more extensive efforts at DNA se- *Present address: Department of Genetics, Case
Western Reserve University, 10900 Euclid Avenue,
vergence from other primates, we need to fit quencing in nonhuman primates has con- Cleveland, OH 44106, USA.
the data to models of sequence divergence firmed the very close evolutionary relation- †To whom correspondence should be addressed. E-
that allow us to distinguish between diver- ship between humans and chimps (2), with an mail: michele_cargill@celeradiagnostics.com
229
1960 12 DECEMBER 2003 VOL 302 SCIENCE www.sciencemag.org
 REPORTS
other public sets and found to be highly the ML estimation procedure corrects for varia- Panther classification system (6, 22). We asked,
consistent (11) (table S1). We used the most tion in base composition; however, if the true for the subset of genes in each functional cate-
conservative set of 7645 genes for which we substitution rate differs across the genome in a gory, whether the distribution of P2 values for
had the highest confidence in orthology and manner that is correlated with GC content, then those genes differed significantly from the P2
sequence annotation (12) (Database S1). we should be able to detect this by simple cor- distribution for the full set of 7645 genes (6)
To identify genes that have undergone relation (6, 12) (Database S2). The synonymous (tables S2 and S3). In this way, we can gain
adaptive protein evolution, we applied two substitution rate was significantly correlated insight into higher-order biological processes
formal statistical tests that fit models of mo- with the following attributes: GC content (0.164, and molecular functions that may be under se-
lecular evolution at the codon level. Both P ⬍ 0.0001), local recombination rate in cM/Mb lective pressure in a given lineage (Tables 1 and
tests fit models of the nucleotide-substitution (21) (0.100, P ⬍ 0.001), and LINE (long inter- 2). The statistical tests of significance are valid
process by maximum likelihood (ML) (13), spersed nuclear element) density (⫺0.091, P ⬍ as formal inferences, and these lead immediately
and both include parameters specifying rates 0.0001). None of these factors was significantly to tentative biological hypotheses, only some of
of synonymous and nonsynonymous substi- correlated with either nonsynonymous substitu- which we describe here.
tution (14– 16). In the first (Model 1), we tion rate or P2-value; however, genes associated In the human lineage, genes involved in
performed a classic test of the null hypothesis with some biological processes, such as olfac- olfaction show a significant tendency to be
of dN/dS ⫽ 1 in the human lineage (17, 18). tion, do show nonrandom associations with under positive selection (PMW ⬍ 0.005) (Ta-
The second model is a modification of the genomic location [P ⬍ 10⫺4, Kolmogorov- ble 1 and Fig. 2). Nearly all the genes clas-
method described by Yang and Nielsen (16), Smirnov (K-S) test] and GC content (P ⬍ 10⫺9, sified to olfaction are olfactory receptors
which allows variation in the dN/dS ratio K-S test). We also verified that segmental dupli- (ORs). It seems likely that the different life-

Downloaded from www.sciencemag.org on August 2, 2010

among lineages and among sites at the same cations were not responsible for distortions in the styles of chimps and humans might have led
time. In this method (Model 2), a likelihood patterns of substitution seen in our tests, mostly to divergent selection pressure on these re-
ratio test of the hypothesis of no positive because genes with close duplicates were under- ceptors. There has been a rapid acceleration
selection is performed by comparing the like- represented in our set because of the requirement of pseudogene formation in human ORs (23),
lihood values for two hypotheses. Under the for strict human-mouse orthology. Interestingly, and the acceleration of apparent amino acid
null hypothesis, it is assumed that all sites are the genes with P2-values ⬍0.05 are overrepre- substitution in pseudogenes could potentially
either neutral (dN/dS ⫽1) or evolve under sented in the Online Mendelian Inheritance in lead to a spurious inference of selection.
negative selection (dN/dS ⬍ 1). Under the Man (OMIM) catalog of genes associated with However, we verified that most of the OR
alternative hypothesis, some of the sites are genetic disease (P ⫽ 0.009), demonstrating the genes in our set are bona fide genes (http://
allowed to evolve with dN ⬎ dS in the human relevance of interspecific comparisons (ftp.ncbi. bioinformatics.weizmann.ac.il/HORDE/), in-
lineage only (Fig. 1). We refer to this as nih.gov/repository/OMIM/morbidmap). dicating that these genes are either undergo-
Model 2, and to the P-value of neutrality as Many of the 7645 genes have been classified ing positive selection or are in the process of
P2 (6). The test based on Model 2 is not as into inferred functional categories based on the pseudogenization (24).
conservative as the test based on Model 1 and
may tend to detect genes with accelerated Fig. 1. Graphical rep-
amino acid substitution rates in humans even resentation of the test
if the average dN/dS rate is not larger than 1. of positive selection
There were 1547 human genes and 1534 (Model 2). The null hy-
chimp genes, which met the criteria for positive pothesis (H0) assumes
all three branches
selection (with dN/dS ⬎1). The neutral null hy- have two classes of
pothesis of Model 1 was rejected for 72 genes amino acid residues:
(0.94% of the tests) at P ⬍ 0.001, 414 genes those that are neutrally evolving ( p1: dN ⫽ dS) and those that are under constraint ( p0: dN/dS⬍
(5.4%) at P ⬍ 0.01, and 1216 genes (15.9%) at 1). The alternative hypothesis (Ha) allows the human lineage to have a subset of sites ( ps)
P ⬍ 0.05 (12). There were six human genes for with accelerated amino acid substitution (dN ⬎ dS).
which the neutral null hypothesis of Model 1
was rejected at P ⬍ 0.05 and dN/dS was greater Fig. 2. P2-value distributions
than 1 (12). The neutral null hypothesis of Model of selected groups of genes.
2 was rejected for 28 genes (0.38%) at P2 ⬍ The plot shows the cumula-
tive fraction of selected bio-
0.001, 178 genes (2.3%) at P2 ⬍ 0.01, and 667
logical processes showing
genes (8.7%) at P2 ⬍ 0.05. The relatively low the excess of cases of signif-
overlap of these sets reflects the different nature icant positive selection in
of the tests. Of the 1547 human genes that ex- genes for olfaction, amino
hibited dN/dS ⬎ 1, only 125 also fell into the acid catabolism, and Mende-
class of 178 human genes with a P2 ⬍ 0.01. lian disease genes (OMIM)
relative to the overall distri-
Similarly, Model 2 can detect cases where a
bution of genes. The distri-
protein has a domain undergoing positive selec- bution of developmental
tion, but the overall dN/dS may not be elevated, genes that do not show a
and thus would be missed by Model 1. For this significant excess is shown
reason, the remainder of the analysis considers for comparison.
only the Model 2 test results.
Before attempting any biological inference
from the results of the statistical tests, it is im-
portant to consider whether attributes like GC
content, repeat density, local recombination rate,
and segmental duplications might affect the rates
and patterns of substitution (19, 20). In principle,
230
www.sciencemag.org SCIENCE VOL 302 12 DECEMBER 2003 1961
 REPORTS
Several other classes of genes (amino acid phenotypic effects. For example, 7 (GSTZ1, which involves the ALDH6A1, BCKDHA, and
catabolism, developmental processes, reproduc- HGD, PAH, ALDH6A1, BCKDHA, PCCB, and PCCB genes, is the primary pathway for energy
tion, neurogenesis, and hearing) show many HAL) of the 16 genes in the amino acid catab- production from muscle protein under starvation
genes with low P2 values, although these classes olism category have P2 values less than 0.05. A conditions (25). For all seven genes, mutations
do not show significant PMW values or contain speculative suggestion is that this signal of pos- have been found that result in human metabolic
fewer than 20 genes (table S1 and Fig. 2). It is itive selection may arise from different dietary disorders, consistent with the idea that natural
possible that individual genes within these cate- habits or pressures in the two lineages. For ex- selection shifted these genes in a manner that is
gories account disproportionately for specific ample, branched-chain amino acid catabolism, relevant to reproductive fitness.
Most of the human developmental genes
Table 1. Biological processes showing the strongest evidence for positive selection. The top panel includes with low P2 values fall into two main cate-
the categories showing the greatest acceleration in human lineage, and the bottom panel includes gories: skeletal development (TLL2, ALPL,
categories with the greatest acceleration in the chimp lineage. BMP4, SDC2, MMP20, and MGP) and neu-
rogenesis (NLGN3, SEMA3B, PLXNC1,
Number of PMW (human/ PMW (chimp/
Biological process NTF3, WNT2, WIF1, EPHB6, NEUROG1,
genes* Model 2)* Model 2)*
and SIM2). In addition, several of the genes
Categories showing the greatest acceleration in human lineage with low P2 values are homeotic transcription
Olfaction 48 0 0.9184 factor genes (CDX4, HOXA5, HOXD4,
Sensory perception 146 (98) 0 (0.026) 0.9691 (0.9079) MEOX2, POU2F3, MIXL1, and PHTF),
Cell surface receptor–mediated signal transduction 505 (464) 0 (0.0386) 0.199 (0.0864) which play key roles in early development.
Chemosensory perception 54 (6) 0 (0.1157) 0.9365 (0.7289)

Downloaded from www.sciencemag.org on August 2, 2010

Nuclear transport 26 0.0003 0.2001 Several genes associated with pregnancy,
G-protein–mediated signaling 252 (211) 0.0003 (0.1205) 0.2526 (0.0773) such as the progesterone receptor (PGR),
Signal transduction 1030 (989) 0.0004 (0.0255) 0.0276 (0.0092) GNRHR, MTNR1A, and PAPPA, appear to
Cell adhesion 132 0.0136 0.3718 exhibit nonneutral divergence between hu-
Ion transport 237 0.0247 0.8025 mans and chimps. PGR is involved not only
Intracellular protein traffic 278 0.0257 0.8099 in maintenance of the uterus, but is also
Transport 391 0.0326 0.7199
Metabolism of cyclic nucleotides 20 0.0408 0.1324 expressed on the cell membrane of sperm,
Amino acid metabolism 78 0.0454 0.0075 where it may play a role in the acrosome
Cation transport 179 0.0458 0.8486 reaction (26), so the physiological basis for
Developmental processes 542 0.0493 0.2322 the adaptive evolution remains unclear.
Hearing 21 0.0494 0.9634 Speech is considered to be a defining char-
acteristic of humans. The forkhead-box P2 tran-
Categories with the greatest acceleration in the chimp lineage scription factor (P2 ⫽ 0.0027) has been impli-
Signal transduction 1030 (989) 0.0004 (0.0255) 0.0276 (0.0092) cated in speech development, and has previously
Amino acid metabolism 78 0.0454 0.0075 been identified as undergoing an unusual hu-
Amino acid transport 23 0.1015 0.0102
Cell proliferation and differentiation 82 0.3116 0.0182
man-specific pattern of substitution (27). Several
Cell structure 174 0.2633 0.0233 genes involved in the development of hearing
Oncogenesis 201 0.3132 0.0267 also appear to have undergone adaptive evolu-
Cell structure and motility 239 0.2208 0.0299 tion in the human lineage, and we speculate that
Purine metabolism 35 0.9127 0.0423 understanding spoken language may have re-
Skeletal development 44 0.2876 0.0438 quired tuning of hearing acuity. The gene with
Mesoderm development 168 0.5813 0.0439
Other oncogenesis 39 0.2777 0.0469
the most significant pattern of human-specific
DNA repair 49 0.9363 0.0477 positive selection is alpha tectorin, whose protein
product plays a vital role in the tectorial mem-
*The number of genes and the PMW values excluding olfactory receptor genes are shown in parentheses.
brane of the inner ear. Single–amino acid poly-
morphisms are associated with familial high-
Table 2. Molecular functions showing the strongest evidence for positive selection. The table includes
only human-accelerated categories, because the only categories accelerated in the chimp lineage are frequency hearing loss (28), and knockout mice
chaperones (P ⫽ 0.0124), cell adhesion molecules (P ⫽ 0.0220), and extracellular matrix (P ⫽ 0.0333). are deaf. These results strongly motivate a de-
tailed assessment of the nature of hearing differ-
Number of PMW (human/ PMW (chimp/ ences between humans and chimpanzees. Other
Molecular function
genes* Model 2)* Model 2)* genes involved in hearing that appear to be under
human-specific selection include DIAPH1,
G protein coupled receptor 199 (153) 0 (0.2533) 0.8689 (0.6776) FOXI1, EYA4, EYA1, and OTOR.
G protein modulator 62 0.0008 0.3776
Receptor 448 0.0030 0.9798 The inference of lineage-specific evolution-
Ion channel 134 0.0043 0.8993 ary acceleration requires a phylogenetic tree. By
Extracellular matrix 97 (95) 0.0120 (0.0178) 0.1482 (0.1593) simply adding mouse to our alignments, we went
Other G protein modulator 32 0.0149 0.4441 from a directionless pairwise comparison of hu-
Extracellular matrix glycoprotein 44 (42) 0.0178 (0.0269) 0.1579 (0.1765) man and chimp to having reasonable ability to
Voltage-gated ion channel 62 0.0219 0.6692 infer common ancestral state, and lineage-specif-
Other hydrolase 95 0.0260 0.4823
Oxygenase 46 0.0303 0.4792 ic changes. These approaches will gain in both
Protein kinase receptor 37 0.0314 0.6911 statistical and biological power as additional pri-
Transporter 214 0.0338 0.1836 mate or other mammalian genomes are se-
Ligand-gated ion channel 45 0.0405 0.9503 quenced, enabling identification of genes that
Microtubule binding motor protein 22 0.0421 0.6385 exhibited accelerated amino acid substitution
Microtubule family cytoskeletal protein 54 0.0467 0.2815 since our most recent common ancestor. Al-
*The number of genes and the PMW values excluding olfactory receptor genes are shown in parentheses. though it is tempting to conclude that this will
231
1962 12 DECEMBER 2003 VOL 302 SCIENCE www.sciencemag.org
 REPORTS
constitute a list of genes that “make us human,” in GenBank under accession codes AY398769- 28. S. Naz et al., J. Med. Genet. 40, 360 (2003).
one has to take a step back to see the gulf that AY421703. 29. The data in this paper were obtained from more
13. J. Felsenstein, J. Mol. Evol. 17, 368 (1981). than 18 million sequencing reads obtained from
exists between understanding at this narrowly 14. N. Goldman, Z. Yang, Mol. Biol. Evol. 11, 725 the Celera Genomics sequencing center in Rock-
focused molecular level and at the organismal (1994). ville, MD. We thank J. Duff, C. Gire, M. A. Rydland,
level. A large number of human genes, when 15. S. V. Muse, B. S. Gaut, Mol. Biol. Evol. 11, 715 (1994). C. Forbes, and B. Small for development and main-
16. Z. Yang, R. Nielsen, Mol. Biol. Evol. 19, 908 (2002). tenance of software systems, laboratory informa-
transformed into mutant yeast or Drosophila, tion management systems, and analysis programs.
17. Z. Yang, R. Nielsen, J. Mol. Evol. 46, 409 (1998).
can rescue the mutant phenotype, but this does 18. Z. Yang, R. Nielsen, Mol. Biol. Evol. 17, 32 (2000). S. Hannenhalli and S. Levy provided particularly
not make these genetically modified organisms 19. I. Hellmann et al., Genome Res. 13, 831 (2003). helpful discussions. C. Aquadro, B. Lazzaro, K. Mon-
20. J. A. Bailey et al., Science 297, 1003 (2002). tooth, T. Schlenke, and P. Wittkopp provided help-
any more human. This study has focused only on ful comments on the manuscript.
21. A. Kong et al., Nature Genet. 31, 241 (2003).
protein-coding genes, and it will require exami-
22. P. D. Thomas et al., Nucleic Acids Res. 31, 334 (2003). Supporting Online Material
nation of regulatory sequences to determine the 23. Y. Gilad, O. Man, S. Pääbo, D. Lancet, Proc. Natl. www.sciencemag.org/cgi/content/full/302/5652/1960/
contribution of regulation of gene expression to Acad. Sci. U.S.A. 100, 3324 (2003). DC1
the evolutionary divergence between humans 24. Y. Gilad, C. D. Bustamante, D. Lancet, S. Paabo, Am. J. Materials and Methods
Hum. Genet. 73, 489 (2003). Tables S1 to S3
and chimps. 25. H. R. Freund, M. Hanani, Nutrition 18, 287 (2002). Databases S1 and S2
Perhaps the best way to understand the rela- 26. S. Gadkar et al., Biol. Reprod. 67, 1327 (2003).
tion between DNA sequence divergence and the 27. W. Enard et al., Nature 418, 869 (2002). 7 July 2003; accepted 24 October 2003
differences between human and chimpanzee
physiology and morphology is to compare these
differences to the variability among humans.
The Proteasome of Mycobacterium

Downloaded from www.sciencemag.org on August 2, 2010

Human-chimp DNA sequence divergence is
roughly 10 times the divergence between ran-
dom pairs of humans. Contrasts that are under tuberculosis Is Required for
way to place human polymorphism in the con-
text of human-specific divergence further em-
power these models to identify molecular targets
Resistance to Nitric Oxide
of natural selection. Evolutionary analysis will K. Heran Darwin,1 Sabine Ehrt,1 José-Carlos Gutierrez-Ramos,2
be extended to include comparison of the X Nadine Weich,2 Carl F. Nathan1,3*
chromosome and autosomes, the impact of local
recombination rates and GC content, codon-us- The production of nitric oxide and other reactive nitrogen intermediates
age patterns, and divergence in regulatory se- (RNI) by macrophages helps to control infection by Mycobacterium tuber-
quences. Additional insight will be gained by culosis (Mtb). However, the protection is imperfect and infection persists.
examining sequence divergence in the context of To identify genes that Mtb requires to resist RNI, we screened 10,100 Mtb
gene-expression differences. The informative- transposon mutants for hypersusceptibility to acidified nitrite. We found 12
ness of all these approaches will increase by mutants with insertions in seven genes representing six pathways, including
inclusion of additional mammalian genome se- the repair of DNA (uvrB) and the synthesis of a flavin cofactor ( fbiC). Five
quences, and realization of the goal to ascribe mutants had insertions in proteasome-associated genes. An Mtb mutant
functional significance to the complex landscape deficient in a presumptive proteasomal adenosine triphosphatase was at-
of our own genome will most effectively be tenuated in mice, and exposure to proteasomal protease inhibitors markedly
made in the context of our close relatives. sensitized wild-type Mtb to RNI. Thus, the mycobacterial proteasome serves
as a defense against oxidative or nitrosative stress.
References and Notes
1. M. C. King, A. C. Wilson, Science 188, 107 (1975). Mtb persistently infects about two billion Thus, mildly acidified nitrite is a physio-
2. Y. Satta, J. Klein, B. Takahata, Mol. Phylogenet. Evol. people. The identification of pathways used logic antimicrobial system. RNI may inflict
14, 259 (2000).
3. F. C. Chen, W.-H. Li, Am. J. Hum. Genet. 68, 444 by the microbe to resist elimination by the not only nitrosative but also oxidative in-
(2001). host immune response may suggest new jury, such as when NO combines with su-
4. I. Ebersberger, D. Metzler, C. Schwarz, S. Pääbo, Am. J. targets for prevention or treatment of tuber- peroxide from bacterial metabolism to gen-
Hum. Genet. 70, 1490 (2002).
5. R. Sakate et al., Genome Res. 13, 1022 (2003).
culosis. During latent infection, the primary erate peroxynitrite (4). Reagent NO kills
6. Detailed materials and methods are available as sup- residence of Mtb is the macrophage. The Mtb with a molar potency exceeding that of
porting material on Science Online. antimicrobial arsenal of the activated mac- most antituberculosis drugs (5, 6). In hu-
7. A total of 201,805 primer pairs were successfully designed rophage includes inducible nitric oxide mans and mice with tuberculosis, macro-
to 23,363 human coding sequences (27.6 Mb).
8. Primer pairs were amplified in 39 female human synthase (iNOS or NOS2) (1). At the acidic phages in infected tissues and airways ex-
individuals (19 African-Americans, 20 Caucasians) pH (ⱕ5.5) prevalent in the phagosome of press enzymatically active iNOS (7–9), and
and 1 male chimpanzee (4X0033, Southwest Nation- activated macrophages (2), nitrite, a major mice lacking iNOS cannot control Mtb in-
al Primate Research Center) by a standard PCR and
sequencing protocols. Trimmed chimp sequences oxidation product of NO, is partially pro- fection (10). Despite the protective effects of
were BLASTed against human exon sequence (9) to tonated to nitrous acid, which dismutates to RNI, a small number of viable mycobacteria
create virtual transcripts. form NO and another radical, 䡠NO2 (3). usually persist for the lifetime of the infected
9. J. C. Venter et al., Science 291, 1304 (2001).
10. R. J. Mural et al., Science 296, 1661 (2002).
host (11) and sometimes resume growth.
11. Mouse-human orthologs were downloaded from Na- 1
Department of Microbiology and Immunology, Weill To identify Mtb genes required for re-
tional Center for Biotechnology Information (NCBI) Medical College of Cornell University, New York, NY sistance against RNI, we screened 10,100
HomoloGene; NCBI Homol_seq_pairs; NCBI Homol- 10021, USA. 2Millennium Pharmaceuticals, 75 Sidney
ogy Map; and Mouse Genome Database, Mouse Ge-
transposon mutants individually for in-
Street, Cambridge, MA 02139, USA. 3Programs in
nome Informatics Web Site, The Jackson Laboratory Immunology and Molecular Biology, Weill Graduate
creased sensitivity to nitrite at pH 5.5 [sup-
(Bar Harbor, ME). School of Medical Sciences of Cornell University, New porting online material (SOM text)].
12. All 7645 alignments in Phylip format (13) and a York, NY 10021, USA. Twelve mutants were hypersensitive. To
flatfile of genes and their associated statistics are
available at http://panther.celera.com/appleraHCM_ *To whom correspondence should be addressed. E- quantify their phenotype, bacteria were ex-
alignments/index.jsp. Sequences have been deposited mail: cnathan@med.cornell.edu posed to pH 5.5 with or without 3 mM
232
www.sciencemag.org SCIENCE VOL 302 12 DECEMBER 2003 1963
233
 SEMINARIO II
PATRONES EVOLUTIVOS: INTERPRETACIONES DEL
REGISTRO FÓSIL
Por Fernando Ventrice, Alicia Massarini, Ignacio M. Soto & Ana Liza Tropea
INTRODUCCIÓN GENERAL
Los orígenes de la humanidad es uno de los temas de la investigación científica que
despierta más pasiones y debates. Muchas hipótesis e ideas que eran aceptadas con entusiasmo en el
pasado han pasado al olvido y otras han surgido a medida que la evidencia se acumula y las técnicas
paleoantropológicas se refinan. Pero las interpretaciones de los fósiles distan mucho de ser
absolutamente objetivas. Las teorías sobre la evolución humana no sólo intentan enmarcar la
evidencia en un contexto lógico basado en las evidencias disponibles, sino que también nos brindan
información valiosa sobre el pensamiento de la época en que fueron formuladas.

Temas
- El registro fósil de los homínidos. Patrones y criterios de interpretación.
- Herramientas para un análisis comparado: elementos de morfología cráneo-facial
- Historia de las teorías y miradas sobre la evolución humana.
- Las evidencias de evolución humana como patrón macroevolutivo.
- Lenguaje y pensamiento simbólico en relación a la evidencia paleontológica.

Tradicionalmente, las inferencias sobre el grado de parentesco existente entre el hombre

moderno y sus parientes cercanos (monos y simios) y fósiles (homíninos) se han basado en el
análisis morfológico a nivel osteológico. Los huesos, en particular los huesos del cráneo, poseen
asociado un alto potencial de fosilización por lo que constituyen la mayoría de los restos del registro
fósil conocido sobre nuestro linaje.
Observe con detenimiento el siguiente esquema sintético de morfología cráneo-facial
comparativo e intente reconocer las estructuras óseas en los ejemplares que se hallarán a su
disposición en el TP.

234
 Por otra parte, los restos líticos confeccionados y utilizados por los homininos también
poseen un alto potencial de conservación asociado. El patrón de distribución geográfico, su
tipología y su variabilidad son rasgos característicos de este registro arqueológico, los cuales se
analizan en conjunto con los rasgos morfológicas presentes en los restos óseos. De manera muy
general, se reconocen en el linaje homínido una serie de “industrias” líticas o “complejos
tecno-culturales” diferentes asociadas a distintas especies. Si bien cada uno de estos complejos es
identificado a través de ciertos componentes diagnósticos, los mismos incluyen una serie variable
de utensilios en cuanto a la forma, el tamaño y la materia prima utilizada. En la figura a
continuación se esquematiza la secuencia de pasos generales que implica el proceso de tallado en
roca para la obtención de utensilios:

235
 Los utensilios más antiguos conocidos datan de aproximadamente 2,6 millones de años
(MA) y se hallaron asociados a los primeros restos óseos asignados al género Homo, en África. Se
trata de cantos rodados tallados en uno o dos planos de manera tal que se genera un filo y se los
denomina choppers o chopping tools. En general, estas primeras herramientas de roca se agrupan
dentro de una “industria” llamada olduvaiense:

Recién hacia los 1,7 MA aparece en África una innovación a nivel de la talla de las materias
primas seleccionadas por los homininos. Se trata de los bifaces, pieza diagnóstica que llevó a la
delimitación de una nueva “industria” lítica, la “industria” acheulense. Estas piezas poseen un
tamaño variable y se caracterizan porque el canto rodado se halla tallado en ambas caras:

Los bifaces se encuentran en el registro arqueológico durante un periodo muy extendido al

igual que en una vasta extensión geográfica (hasta en Europa y Asia), por lo tanto se las asocia a
distintas especies de homininos.
A medida que nos acercamos al millón de años de antigüedad, el nutrido registro
arqueológico permitió la definición de secuencias temporales de muchas industrias, muy diversas,
por lo general con especificidad regional.
Desde comienzos del Paleolítico Superior, hacia los 40.000 años AP, se observa una
aceleración de la evolución de las técnicas de subsistencia conjuntamente con la emergencia del
pensamiento simbólico (evidenciado por las múltiples expresiones de arte). Una innovación
característica a nivel de la talla de las rocas es la talla de tipo microlaminar que permite obtener un
gran rendimiento de utensilios a partir de una cantidad reducida de materia prima. Por otra parte, se
registra el uso intensivo del hueso como materia prima para la talla. Todas estas “industrias” se
asocian a la especie Homo sapiens. Se ejemplifican a continuación algunas de esas piezas:

236
ACTIVIDADES A REALIZAR:
Su grupo dispondrá de información sobre distintos fósiles de homínidos y patrones
paleoambientales y temporales de distribución. A partir de dicha información y de los elementos
descritos anteriormente:
1. Desarrolle una hipótesis evolutiva y confeccione un esquema de relaciones entre los
especímenes y el hombre.
2. Especifique el número de especies que quedan conformadas y las características elegidas
como claves evolutivas y criterios de agrupamiento.

3. Actividad Complementaria: lectura y discusión de las siguientes preguntas:

- Tattersall, I. 2005. Once we were not alone. Scientific American 25-32.
3.1. ¿Cuál es la edad de los fósiles más antiguos pertenecientes al género Australopithecus? ¿Y
del género Homo?
3.2. ¿Qué planteaba la hipótesis de especie única? ¿Qué factores contribuían al mantenimiento
de esta línea de pensamiento?
3.3. ¿Cómo afectaron los descubrimientos efectuados a partir de 1970 a la concepción que se
tenía del modo de evolución del linaje humano? ¿Cómo es ahora el panorama atribuible a la
diversidad de homínidos hace 1.8 millones de años?
3.4. ¿Qué rol se le atribuye a Neandertal (y a las poblaciones asiáticas de H. erectus) en una
visión lineal de la evolución? ¿Qué propone la teoría arbustiva?
3.5. ¿Qué propone Tattersall acerca de los neandertales? ¿Qué diferencias se observan en la
coexistencia ocurrida entre H. sapiens y H. neanderthalensis entre Medio Oriente y Europa?
¿Qué propone el autor acerca del resultado de esas interacciones?
3.6. En octubre de 2004 se describió a una nueva especie de homínido: Homo floresiensis. Esta
especie existió hasta hace 13.000 años en una isla del sudeste asiático. ¿Cómo repercute este
descubrimiento en el modelo sostenido por Tattersal?
3.7. ¿Cuál habría sido según Tattersall la característica clave del éxito de H. sapiens y cómo se
habría establecido? ¿Cómo se aplican en este caso los conceptos de exaptación y de
emergencia?
3.8. ¿Cómo interpreta Tattersall el hecho que los patrones de comportamiento moderno de los
humanos, que denotan la existencia de pensamiento simbólico, se establecieron mucho
tiempo después que las características anatómicas típicas de H. sapiens?

237
BIBLIOGRAFÍA COMPLEMENTARIA

• Domínguez-Rodrigo, M. 2002. Hunting and scavenging by early humans: The state of debate. Journal of
World Prehistory 16:1-54.
• Foley, R. 1993. Causes and Consequences in Human Evolution. J. Roy. Anthrop. Inst. 1:67-86.
• Stiner, M. C. 2002. Carnivory, coevolution and the geographic spread of the genus Homo. Journal of
Archaeological Research 10: 31-68.
• Klein, R.G. 2003. Whither the Neanderthals? Science 229:1525-1527.
• McBrearty, S.; Brooks, A.S. 2000. The revolution that wasn’t: a new interpretation of the origin of modern
human behavior. J Hum Evol 39:453-563.
• d'Errico, F. 2003. The invisible frontier. A multiple species model for the origin of behavioral modernity.
Evolutionary Anthropology 12 (4):188-202.

238
 EMERGENCE originally published in 2003

TODAY WE TAKE FOR GRANTED THAT HOMO SAPIENS

FOUR MILLION YEARS MANY HOMINID SPECIES

ONCE we

SHARING A SINGLE LANDSCAPE, four kinds of hominids lived about 1.8 million years ago in what is now part of northern Kenya.
Although paleoanthropologists have no idea how— or if— these different species interacted, they do know that Paranthropus boisei,
Homo rudolfensis, H. habilis and H. ergaster foraged in the same area around Lake Turkana.

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25 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE AUGUST 2005
COPYRIGHT 2005 SCIENTIFIC AMERICAN, INC.
IS THE ONLY HOMINID ON EARTH. YET FOR AT LEAST
SHARED THE PLANET. WHAT MAKES US DIFFERENT?

were not alone

By Ian Tattersall • Paintings by Jay H. Matternes

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26 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE AUGUST 2005
COPYRIGHT 2005 SCIENTIFIC AMERICAN, INC.
Homo sapiens has had the earth to itself
for the past 25,000 years or so, free and years ago in what is now northern Kenya, tinct geographical regions offer some in-
clear of competition from other mem- that the single-species hypothesis was triguing insights.
bers of the hominid family. This period abandoned. Yet even then, paleoanthro-
has evidently been long enough for us to pologists continued to cleave to a rather A Suite of Species
have developed a profound feeling that minimalist interpretation of the fossil F R O M T H E B E G I N N I N G , almost from
being alone in the world is an entirely record. Their tendency was to downplay the very moment the earliest hominid
natural and appropriate state of affairs. the number of species and to group to- biped— the first “australopith”— made
So natural and appropriate, indeed, gether distinctively different fossils un- its initial hesitant steps away from the
that during the 1950s and 1960s a der single, uninformative epithets such forest depths, we have evidence for hom-
school of thought emerged that claimed, as “archaic Homo sapiens.” As a result, inid diversity. The oldest-known poten-
in essence, that only one species of hom- they tended to lose sight of the fact that tial hominid is Sahelanthropus tchaden-
inid could have existed at a time because many kinds of hominids had regularly sis, represented by a cranium from the
there was simply no ecological space on contrived to coexist. central-western country of Chad [see il-
the planet for more than one culture- Although the minimalist tendency lustration on page 26]. Better known is
bearing species. The “single-species hy- persists, recent discoveries and fossil Australopithecus anamensis, from sites
pothesis” was never very convincing— reappraisals make clear that the biolog- in northern Kenya that are about 4.2
even in terms of the rather sparse homi- ical history of hominids resembles that million years old.
nid fossil record of 40 years ago. But the of most other successful animal families. A. anamensis looks reassuringly simi-
implicit scenario of the slow, single- It is marked by diversity rather than by lar to the 3.8- to 3.0-million-year-old
minded transformation of the bent and linear progression. Despite this rich his- Australopithecus afarensis, a small-
benighted ancestral hominid into the tory— during which hominid species de- brained, big-faced bipedal species to
graceful and gifted modern H. sapiens veloped and lived together and compet- which the famous “Lucy” belonged.
proved powerfully seductive— as fables ed and rose and fell— H. sapiens ulti- Many remnants of A. afarensis have
of frogs becoming princes always are. mately emerged as the sole hominid. The been found in various eastern African
So seductive that it was only in the reasons for this are generally unknow- sites, but some researchers have suggest-
late 1970s, following the discovery of in- able, but different interactions between ed that the mass of fossils described as A.
controvertible fossil evidence that hom- the last coexisting hominids— H. sapiens afarensis may contain more than one
inid species coexisted some 1.8 million and H. neanderthalensis— in two dis- species, and it is only a matter of time

PARANTHROPUS BOISEI HOMO RUDOLFENSIS

had massive jaws, was a relatively
equipped with huge large-brained
grinding teeth for a hominid, typified by
presumed vegetarian the famous KNM-ER
diet. Its skull is 1470 cranium. Its
accordingly strongly skull was distinct
built, but it is not from the apparently
known if in body size it smaller-brained H.
was significantly larger habilis, but its body
than the “gracile” proportions are
australopiths. effectively unknown.

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27 SCIENTIFIC AMERICAN EXCLUSIVE ONLINE ISSUE AUGUST 2005
COPYRIGHT 2005 SCIENTIFIC AMERICAN, INC.
until the subject is raised again. In any tinctive P. robustus and possibly a close- could wish for a better record of this
event, A. afarensis was not alone in ly related second species, P. crassidens. movement, and particularly of its dat-
Africa. A distinctive jaw, from an aus- I apologize for inflicting this long list ing, but there are indications that hom-
tralopith named A. bahrelghazali, was of names on readers, but in fact it actu- inids of some kind had reached China
found in 1995 in Chad. It is probably ally underestimates the number of aus- and Java by about 1.8 million years ago.
between 3.5 and 3.0 million years old tralopith species that existed. What is A lower jaw that may be about the same
and is thus roughly coeval with Lucy, as more, scientists don’t know how long age from Dmanisi in ex-Soviet Georgia
is the recently named new form Kenyan- each of these creatures lasted. Neverthe- is different from anything else yet found
thropus platyops. less, even if average species longevity [see “Out of Africa Again ... and Again?”
In southern Africa, scientists reported was only a few hundred thousand years, by Ian Tattersall; SCIENTIFIC AMERICAN,
evidence in 1999 of another primitive it is clear that from the very beginning April 1997]. By the million-year mark
bipedal hominid species. As yet un- the continent of Africa was at least pe- H. erectus was established in both Java
named and undescribed, this distinctive riodically— and most likely continual- and China, and it is possible that a more
form is 3.3 million years old. At about ly— host to multiple kinds of hominids. robust hominid species was present in
three million years ago, the same region The appearance of the genus Homo Java as well. At the other end of the
begins to yield fossils of A. africanus, the did nothing to perturb this pattern. The Eurasian continent, the oldest-known
first australopith to be discovered (in 2.5- to 1.8-million-year-old fossils from European hominid fragments— from
1924). This species may have persisted eastern and southern Africa that an- about 800,000 years ago— are highly
until not much more than two million nounce the earliest appearance of Homo distinctive and have been dubbed H. an-
years ago. A 2.5-million-year-old species are an oddly assorted lot and probably a tecessor by their Spanish discoverers.
from Ethiopia, named Australopithecus lot more diverse than their conventional About 600,000 years ago, in Africa,
garhi in 1999, is claimed to fall in an in- assignment to the two species H. habilis we begin to pick up evidence for H. hei-
termediate position between A. afaren- and H. rudolfensis indicates. Still, at delbergensis, a species also seen at sites
sis, on the one hand, and a larger group Kenya’s East Turkana, in the period be- in Europe— and possibly China— be-
that includes more recent australopiths tween 1.9 and 1.8 million years ago, tween 500,000 to 200,000 years ago. As
and Homo, on the other. Almost exact- these two species were joined not only we learn more about H. heidelbergensis,
ly the same age is the first representative by the ubiquitous P. boisei but by H. er- we are likely to find that more than one
of the “robust” group of australopiths, gaster, the first hominid of essentially species is actually represented in this
Paranthropus aethiopicus. This early modern body form. Here, then, is evi- group of fossils. In Europe, H. heidel-
form is best known from the 2.5-mil- dence for four hominid species sharing bergensis or a relative gave rise to an en-
lion-year-old “Black Skull” of northern not just the same continent but the same demic group of hominids whose best-
Kenya, and in the period between about landscape [see illustration on previous known representative was H. nean-
2 and 1.4 million years ago the robusts page and below]. derthalensis, a European and western
were represented all over eastern Africa The first exodus of hominids from Asian species that flourished between
by the familiar P. boisei. In South Africa, Africa, presumably in the form of H. er- about 200,000 and 30,000 years ago.
during the period around 1.6 million gaster or a close relative, opened a vast The sparse record from Africa suggests
years ago, the robusts included the dis- prospect for further diversification. One that at this time independent develop-

HOMO HABILIS HOMO ERGASTER,

(“handy man”) was sometimes called “African
so named because it H. erectus,” had a high,
was thought to be the rounded cranium and a
maker of the 1.8- skeleton broadly similar
million-year-old to that of modern
stone tools humans. Although H.
discovered at Olduvai ergaster clearly ate meat,
Gorge in Tanzania. its chewing teeth are
This hominid relatively small. The best
fashioned sharp specimen of this hominid
flakes by banging is that of an adolescent
one rock cobble from about 1.6 million
against another. years ago known as
Turkana boy.

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TUC D’AUDOUBERT CAVE in France was entered sometime between perhaps
11,000 and 13,000 years ago by H. sapiens, also called Cro Magnons, who
sculpted small clay bison in a recess almost a mile underground.

ments were taking place there, too— in- involving the cop-out of stuffing all vari- than gradual accretions. Over the past
cluding the emergence of H. sapiens. ants of Homo of the past half a million five million years, new hominid species
And in Java, possible H. erectus fossils or even two million years into the species have regularly emerged, competed, co-
from Ngandong were dated to around H. sapiens. existed, colonized new environments
40,000 years ago, implying that this area My own view, in contrast, is that the and succeeded— or failed. We have only
had its own indigenous hominid evolu- 20 or so hominid species invoked (if not the dimmest of perceptions of how this
tionary history for perhaps millions of named) above represent a minimum es- dramatic history of innovation and in-
years as well. timate. Not only is the human fossil teraction unfolded, but it is already evi-
The picture of hominid evolution just record as we know it full of largely un- dent that our species, far from being the
sketched is a far cry from the “Australo- acknowledged morphological indica- pinnacle of the hominid evolutionary
pithecus africanus begat Homo erectus tions of diversity, but it would be rash to tree, is simply one more of its many ter-
begat Homo sapiens” scenario that pre- claim that every hominid species that minal twigs.
vailed 40 years ago— and it is, of course, ever existed is represented in one fossil
based to a great extent on fossils that collection or another. And even if only The Roots of Our Solitude
have been discovered since that time. the latter is true, it is still clear that the A L T H O U G H T H I S is all true, H. sapi-
Yet the dead hand of linear thinking still story of human evolution has not been ens embodies something that is undeni-
lies heavily on paleoanthropology, and one of a lone hero’s linear struggle. ably unusual and is neatly captured by
even today quite a few of my colleagues Instead it has been the story of na- the fact that we are alone in the world
would argue that this scenario overesti- ture’s tinkering: of repeated evolution- today. Whatever that something is, it is
mates diversity. There are various ways ary experiments. Our biological history related to how we interact with the ex-
of simplifying the picture, most of them has been one of sporadic events rather ternal world: it is behavioral, which

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 HOMINIDS of modern body form most
likely emerged in Africa around 150,000
years ago and coexisted with other
hominids for a time before emerging as
the only species of our family. Until
about 30,000 years ago, they overlapped
with H. neanderthalensis (left) in Europe
and in the Levant, and they may have
been contemporaneous with the
H. erectus (right) then living in Java.

means that we have to look to our ar- who did the same, the Neandertals fur- lack the “grave goods” that would attest
chaeological record to find evidence of nish us with a particularly instructive to ritual and belief in an afterlife. The
it. This record begins some 2.5 million yardstick by which to judge our own Neandertals, in other words, though ad-
years ago with the production of the first uniqueness. The stoneworking skills of mirable in many ways and for a long
recognizable stone tools: simple sharp the Neandertals were impressive, if time successful in the difficult circum-
flakes chipped from parent “cores.” We somewhat stereotyped, but they rarely if stances of the late ice ages, lacked the
don’t know exactly who the inventor ever made tools from other preservable spark of creativity that, in the end, dis-
was, but chances are that he or she was materials. And many archaeologists tinguished H. sapiens.
something we might call an australopith. question the sophistication of their hunt- Although the source of H. sapiens as
This landmark innovation represent- ing skills. a physical entity is obscure, most evi-
ed a major cognitive leap and had pro- Further, despite misleading early ac- dence points to an African origin perhaps
found long-term consequences for hom- counts of bizarre Neandertal “bear between 150,000 and 200,000 years
inids. It also inaugurated a pattern of cults” and other rituals, no substantial ago. Modern behavior patterns did not
highly intermittent technological change. evidence has been found for symbolic emerge until much later. The best evi-
It was a full million years before the next behaviors among these hominids or for dence comes from Israel and its sur-
significant technological innovation the production of symbolic objects— cer- rounding environs, where Neandertals
came along: the creation about 1.5 mil- tainly not before contact had been made lived about 200,000 years ago or per-
lion years ago, probably by H. ergaster, with modern humans. Even the occa- haps even earlier. By about 100,000
of the hand ax. These symmetrical im- sional Neandertal practice of burying years ago, they had been joined by
plements, shaped from large stone cores, the dead may have been simply a way of anatomically modern H. sapiens, and
were the first tools to conform to a “men- discouraging hyenas from making in- the remarkable thing is that the tools
tal template” that existed in the tool- cursions into their living spaces or have and sites the two hominid species left be-
maker’s mind. This template remained a similar mundane explanation. This hind are essentially identical. As far as
essentially unchanged for another mil- view arises because Neandertal burials can be told, these two hominids behaved
lion years or more, until the invention of
“prepared-core” tools by H. heidelber- IAN TATTERSALL and JAY H. MATTERNES have worked together since the early 1990s, no-
THE AUTHOR AND THE ARTIST

gensis or a relative. Here a stone core was tably on the Hall of Human Biology and Evolution at the American Museum of Natural His-
elaborately shaped in such a way that a tory in New York City and at the Gunma Museum of Natural History in Tomioka, Japan (where
single blow would detach what was an the Tuc d’Audoubert mural on the opposite page is installed). Tattersall was born in England
effectively finished implement. and raised in East Africa. He is a curator in the department of anthropology at the Ameri-
Among the most accomplished practi- can Museum of Natural History. His books include Becoming Human: Evolution and Human
tioners of prepared-core technology Uniqueness (Harvest Books, 1999) and The Last Neanderthal: The Rise, Success, and Mys-
were the large-brained, big-faced and terious Extinction of Our Closest Human Relatives (Westview Press, 1999, revised).
low-skulled Neandertals, who occupied Matternes is an artist and sculptor who has for more than 40 years specialized in fos-
Europe and western Asia until about sil primates and hominids. In addition to his museum murals, he is well known for his illus-
30,000 years ago. Because they left an trations for books, periodicals and television, including Time/Life Books and National Geo-
excellent record of themselves and were graphic. The research for his depictions has taken him to many parts of the U.S., Canada,
abruptly replaced by modern humans Mexico, France, Colombia and Africa.

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 0 H. sapiens (Worldwide)

H. neanderthalensis
(Europe and Western Asia) in similar ways despite their anatomical
differences. And as long as they did so,
they somehow contrived to share the
H. heidelbergensis (throughout Old World)
Levantine environment.
The situation in Europe could hardly
H. erectus (Eastern Asia) be more different. The earliest H. sapi-
1 H. antecessor
(Spain) ens sites there date from only about
40,000 years ago, and just 10,000 or so
years later the formerly ubiquitous Ne-
andertals were gone. Significantly, the
H. sapiens who invaded Europe brought
H. habilis with them abundant evidence of a fully
(Sub-Saharan Africa) formed and unprecedented modern sen-
K. rudolfensis
(Eastern Africa) sibility. Not only did they possess a new
“Upper Paleolithic” stoneworking tech-
2
Homo ergaster P. robustus P. boisei nology based on the production of mul-
(Eastern Africa) (South Africa) (Eastern Africa) tiple long, thin blades from cylindrical
cores, but they made tools from bone
Au. africanus and antler, with an exquisite sensitivity
Millions of Years Ago

(South Africa) Paranthropus

aethiopicus to the properties of these materials.
Au. garhi (Eastern Africa) Even more significant, they brought
(Ethiopia) with them art, in the form of carvings,
engravings and spectacular cave paint-
3 ings; they kept records on bone and
stone plaques; they made music on wind
instruments; they crafted intricate per-
Au. bahrelghazali sonal adornments; they afforded some
(Chad) of their dead elaborate burials with
grave goods (hinting at social stratifica-
tion in addition to belief in an afterlife,
Kenyanthropus Au. afarensis for not all burials were equally fancy);
platyops (Ethiopia and Australopithecus
4 (Kenya) anamensis
and their living sites were highly orga-
Tanzania)
(Kenya) nized, with evidence of sophisticated
hunting and fishing. The pattern of in-
termittent technological innovation was
gone, replaced by constant refinement.
Clearly, these people were us.

Competing Scenarios
Ardipithecus ramidus I N A L L T H E S E W A Y S , early Upper Pa-
5 (Ethiopia)
leolithic people contrasted dramatically
with the Neandertals. Some Neandertals
in Europe seem to have picked up new
ways of doing things from the arriving
H. sapiens, but we have no direct clues
as to the nature of the interaction be-
Orrorin tugenensis tween the two species. In light of the Ne-
(Kenya)
andertals’ rapid disappearance and of
PATRICIA J. WYNNE (drawings)

6
the appalling subsequent record of H.
sapiens, though, we can reasonably sur-
SPECULATIVE FAMILY TREE shows the variety of hominid mise that such interactions were rarely
species that have populated the planet— some identified by happy for the former. Certainly the re-
only a fragment, others known to exist for a specific time
period (solid lines). The emergence of H. sapiens has not peated pattern found at archaeological
been a single, linear transformation of one species into Sahelanthropus sites is one of short-term replacement,
another but rather a meandering, multifaceted evolution. tchadensis and there is no convincing biological ev-
(Chad)
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 The pattern of intermittent technological innovation
was gone, replaced by constant refinement.
Clearly, these people were us.

idence of any intermixing of peoples in see that, profound as the consequences sufficiently advantageous, this behav-
Europe. of achieving symbolic thought may have ioral novelty could then have spread
In the Levant, the coexistence ceased— been, the process whereby it came about rapidly by cultural contact among pop-
after about 60,000 years or so— at right was unexceptional. ulations that already had the potential to
about the time that Upper Paleolithic– We have no idea at present how the acquire it. No population replacement
like tools began to appear. About 40,000 modern human brain converts a mass of would have been necessary to spread the
years ago the Neandertals of the Levant electrical and chemical discharges into capability worldwide.
yielded to a presumably culturally rich what we experience as consciousness. It is impossible to be sure what this in-
H. sapiens, just as their European coun- We do know, however, that somehow novation might have been, but the best
terparts had. our lineage passed to symbolic thought current bet is that it was the invention of
The key to the difference between the from some nonsymbolic precursor state. language. For language is not simply the
European and the Levantine scenarios The only plausible possibility is that medium by which we express our ideas
lies, most probably, in the emergence of with the arrival of anatomically modern and experiences to one another. Rather
modern cognition— which, it is reason- H. sapiens, existing exaptations were it is fundamental to the thought process
able to assume, is equivalent to the ad- fortuitously linked by a relatively minor itself. It involves categorizing and nam-
vent of symbolic thought. Business had genetic innovation to create an unprece- ing objects and sensations in the outer
continued more or less as usual right dented potential. and inner worlds and making associa-
through the appearance of modern bone Yet even in principle this deduced sce- tions between resulting mental symbols.
structure, and only later, with the ac- nario cannot be the full story, because It is, in effect, impossible for us to con-
quisition of fully modern behavior pat- anatomically modern humans behaved ceive of thought (as we are familiar with
terns, did H. sapiens become complete- archaically for a long time before adopt- it) in the absence of language, and it is
ly intolerant of competition from its ing modern behaviors. That discrepan- the ability to form mental symbols that
nearest— and, evidently, not its dearest— cy may be the result of the late appear- is the fount of our creativity. Only when
co-inhabitors. ance of some key hardwired innovation we are able to create such symbols can
To understand how this change in sen- not reflected in the skeleton, which is all we recombine them and ask such ques-
sibility occurred, we have to recall cer- that fossilizes. But this seems unlikely, tions as “What if...?”
tain things about the evolutionary pro- because it would have necessitated a We do not know exactly how lan-
cess. First, as in this case, all innovations wholesale Old World–wide replacement guage might have emerged in one local
must necessarily arise within preexisting of hominid populations in a very short population of H. sapiens, although lin-
species— for where else can they do so? time, something for which there is no guists have speculated widely. But we do
Second, many novelties arise as “exap- evidence. know that a creature armed with sym-
tations,” features acquired in one con- It is much more likely that the modern bolic skills is a formidable competitor—
text before (often long before) being co- human capacity was born at— or close and not necessarily an entirely rational
opted in a different one. For example, to— the origin of H. sapiens, as an abili- one, as the rest of the living world, in-
hominids possessed essentially modern ty that lay fallow until it was activated cluding H. neanderthalensis, has discov-
vocal tracts for hundreds of thousands by a cultural stimulus of some kind. If ered to its cost.
of years before the behavioral record
gives us any reason to believe that they MORE TO E XPLORE
employed the articulate speech that the Dark Caves, Bright Visions: Life in Ice Age Europe. Randall White. W. W. Norton/American Museum
of Natural History, 1986.
peculiar form of this tract permits.
Language and Species. Reprint edition. Derek Bickerton. University of Chicago Press, 1992.
And finally, it is important to bear in
The Fossil Trail: How We Know What We Think We Know about Human Evolution. Ian Tattersall.
mind the phenomenon of emergence— Oxford University Press, 1995.
the notion that a chance coincidence Getting Here: The Story of Human Evolution. Updated edition. William Howells. Compass Press,
gives rise to something totally unexpect- 1997.
ed. The classic scientific example in this African Exodus: The Origins of Modern Humanity. Reprint edition. Christopher Stringer and
Robin McKie. Henry Holt, 1998.
regard is water, whose properties are
The Origin and Diversification of Language. Edited by Nina G. Jablonski and Leslie C. Aiello.
wholly unpredicted by those of hydro- University of California Press, 1998.
gen and oxygen atoms alone. If we com- The Last Neanderthal: The Rise, Success and Mysterious Extinction of Our Closest Human
bine these various observations, we can Relatives. Revised edition. Ian Tattersall. Westview Press, 1999.

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247
 SEMINARIO III
SURGIMIENTO DEL HOMBRE MODERNO, OLEADAS MIGRATORIAS Y
EVOLUCIÓN DE Homo sapiens
Por Alicia Massarini, Ignacio M. Soto & Ana Liza Tropea

INTRODUCCIÓN GENERAL

Homo sapiens es, actualmente, una especie cosmopolita. La distribución actual responde a
un fenómeno que empezó hace millones de años con la/s población/es de homínidos que
abandonaron por primera vez África, el continente origen de nuestro linaje. El proceso de
poblamiento de nuestro planeta interesa tanto por sus causas como por sus consecuencias y es uno
de los aspectos en donde la adaptabilidad de nuestra especie queda más evidenciada. Sin embargo,
la reconstrucción del patrón de migraciones no se comprende plenamente y actualmente es objeto
de intenso debate.

TEMAS:

- Surgimiento del Hombre Moderno (género Homo).

- Modelos teóricos de surgimiento: “modelo Multirregional” y “modelo Fuera de África”.
Evidencias que sustentan cada modelo. Controversias asociadas.
- Poblamiento del Viejo Mundo. Oleadas migratorias durante el Pleistoceno Medio y
Superior.
- La evolución operando en la actualidad sobre Homo sapiens.

ACTIVIDADES A REALIZAR:

A partir de la bibliografía de lectura obligatoria se responderán y discutirán las siguientes preguntas:

Wilson, A. C.; Cann, R. L.; Origen africano reciente de los humanos; Investigación y
Ciencia; Junio de 1992.

1.1. ¿Qué ventajas tendría según los autores, la utilización de datos moleculares respecto de los
datos paleontológicos tradicionales para la reconstrucción de historias de parentesco? ¿En qué
medida el ejemplo presentado de Ramaphitecus ilustra esta controversia?

1.2. ¿Por qué se utiliza ADN mitocondrial para el estudio de la evolución reciente de los humanos?
¿Cuáles son sus ventajas respecto del ADN nuclear? ¿A qué se refiere la metáfora “Eva
mitocondrial”? ¿Con qué criterios Kocher (1988) seleccionó un árbol de ADNmt entre los
múltiples posibles? ¿Qué nueva información proporcionó el estudio comparado de ADNmt de
chimpancés y humanos?

1.3. ¿Qué se observó cuando los autores utilizaron una muestra que incluía 182 tipos diferentes de
ADNmt? ¿Qué información aporta este tipo de estudios respecto de la colonización de distintas
regiones por Homo sapiens? ¿Qué sugieren acerca del concepto clásico de raza? ¿Y acerca del
escenario geográfico donde ocurrió el origen de Homo sapiens?

248
1.4. ¿Con qué criterios se estableció la datación del origen de nuestra especie? ¿Podrían relacionar
este aspecto del estudio con la discusión planteada en la introducción de trabajo acerco de la
objetividad de los datos moleculares? ¿Qué relación existe entre la hipótesis de Eva
mitocondrial y las evidencias fósiles disponibles actualmente?

1.5. ¿Qué críticas hacen los autores al modelo multirregional? ¿Qué explicaciones proponen para el
desplazamiento sin hibridación de las antiguas poblaciones de homínidos por Homo sapiens?
¿Qué nuevas perspectivas podrán ampliar la comprensión de este problema?

Thorne, A. G.; Wolpoff, M. H.; Evolución Multirregional de los humanos; Investigación y

Ciencia; Junio 1992.

2.1. ¿Cómo presentan los autores su hipótesis sobre el origen del hombre moderno? ¿Cuál es la
analogía que proponen para comparar los dos modelos en disputa? ¿Cuál es la opinión de los
autores sobre los distintos tipos de datos que se utilizan para interpretar el problema?

2.2. ¿Cuáles son las premisas que según los autores deberían cumplirse en el modelo Eva
mitocondrial? ¿Por qué se afirma que el registro arqueológico estaría contradiciendo las
predicciones del modelo de Eva?

2.3. ¿Qué se propone acerca del camino anatómico a nivel regional que supone el modelo de Eva
mitocondrial? ¿Por qué se propone que si el modelo de Eva fuera correcto, la continuidad de las
formas a nivel regional debería ser “superficial”?

2.4. ¿Cómo interpretan los autores las relaciones filogenéticas existentes entre neandertales y Homo
sapiens?

2.5. Según los autores: ¿qué se espera encontrar en África si la hipótesis de Eva fuera correcta?
¿Cómo interpretan las evidencias existentes en este continente? ¿Cuál es la interpretación
alternativa a los datos de ADN mitocondrial, en el caso de afirmar que hubo hibridación entre
poblaciones locales y migrantes?

2.6. ¿Cómo afectaría a la datación del origen de Homo sapiens la pérdida azrosa de linajes de
ADNmt? ¿Por qué se propone que debe considerarse la historia demográfica de las poblaciones?
¿Qué otras objeciones se plantean al reloj molecular mitocondrial? ¿Cómo reinterpretan e
incorporan estos autores las evidencias moleculares en relación con su hipótesis?

Balter, M. 2005. Are Humans Still Evolving? Science 309:234-237.

3.1. ¿Cuál sería la relación entre el preconcepto de que la evolución se ha detenido en nuestra
especie y la Escala del Ser?

3.2. ¿Seguimos evolucionando los humanos? ¿Por procesos selectivos o por deriva? Comente
ejemplos de ambos procesos.

3.3. ¿Cuáles son las funciones o efectos de los genes con señales de selección reciente comentados
en el trabajo?

249
3.4. ¿Cuáles son las consecuencias evolutivas del desarrollo cultural y tecnológico de los humanos?

3.5. Discuta el futuro de la evolución humana, la predicción de los fenotipos por parte de la
Biología, y los posibles patrones macroevolutivos en nuestro linaje.

SÍNTESIS
Es preciso comprender que ambos modelos son, actualmente, los extremos de una gama
muy diversa de modelos que intentan explicar el "cómo" del surgimiento del hombre moderno y su
distribución posterior, revelada a través del registro fósil.
A partir de la discusión de estos trabajos fundacionales, y a modo de síntesis, los alumnos
deberían llegar a comparar ambos modelos según los siguientes criterios: (1) lugar geográfico
originario de Homo sapiens; (2) población ancestral; (3) edad de la especie humana; (4) tipos de
evidencias utilizadas; (5) posición filogenética de neandertales; (6) dinámica de poblamiento a nivel
del viejo mundo; (7) mirada macroevolutiva subyacente.

BIBLIOGRAFÍA COMPLEMENTARIA

• Tattersall, I. 2003. Out of Africa again…and again? Scientific American.

• Stringer, C. B. 1991. ¿Está en África nuestro Origen? Investigación y Ciencia.

• Stringer, C. B. 2001. Modern Human Origins – Distinguishing the Models. African Archaeological Review
18 (2).
• Templeton, A. 2007. Genetics and recent human evolution. Evolution 61-7: 1507–1519.

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 N e w s Fo c u s

The goal of much of modern medicine and culture is effectively to stop evolution. Is that happening?

Are Humans Still Evolving?

The news made headlines around the world: ral selection and other evolutionary mecha- In that sense, in the developed world, human
Blonds were going extinct. According to nisms. Some say the question itself betrays a evolution has stopped.”
CNN and other media, a World Health misunderstanding of how evolution works. Yet millions of people in developing
Organization (WHO) study concluded that “The very notion that … we might not be countries continue to live under the com-
the gene for blond hair, which was evolving derives from a belief that all other bined stresses of poverty and disease. Under
described as recessive to dominant genes life forms were merely stages on the way to these conditions, even skeptics of ongoing
for dark hair, would disappear in human evolution agree that natural selec-
200 years. The BBC announced tion may be favoring genes that confer
that the last natural blond would resistance to disease or enhance repro-
be born in Finland and suggested ductive f itness in other ways. Indeed,
that those who dyed their hair researchers are now tracking how deadly
might be to blame, because “bot- maladies such as AIDS and malaria exert
tle blonds” were apparently selective pressure on people today. “As long
more attractive to the opposite as some people die before reproducing or
sex than natural blonds were and reaching reproductive age, selection is
thus had more children. likely to be acting,” says geneticist Chris
Fortunately for blonds, the Tyler-Smith of the Sanger Institute near
whole story turned out to be a Cambridge, United Kingdom.
hoax—“a pigment of the imag- Even in developed countries, where sur-
ination,” as the Times of India vival tends to be prolonged for almost all,
later put it. WHO announced recent studies suggest that there are still
that it had never conducted genetic differences among people in fertil-
such a study, and hair color is ity and reproductive fitness, an indication
probably determined by several Modern mismatch. Overbite is widespread among modern that natural selection is operating. “The
genes that do not act in a sim- humans, but evolution may not be to blame. question ‘Are humans still evolving?’
ple dominant-recessive rela- should be rephrased as ‘Do all people have
tionship. The story, which may have orig- the appearance of humans as the intended the same number of children?’ ” says
inally sprung from a German women’s end point,” says primatologist Mary Pavelka Pavelka. “The answer is that we do not make
magazine, apparently simply leaped from of the University of Calgary in Canada. equal contributions to the next generation,
one media outlet to another. But other scientists point out that in and thus we are still evolving.”
Although the story was untrue, the ease developed countries, culture, technology, Over the past few years, a wealth of new
CREDITS (TOP TO BOTTOM): GETTY IMAGES; M. MÖLLENBERG/ZEFA/CORBIS
with which it spread reflects popular fascina- and especially medical advances have data has begun to illuminate how natural
tion with the evolutionary future of our changed the evolutionary rules, from sur- selection has shaped—and may still be
species, as well as the media’s appetite for vival of the fittest to the survival of nearly shaping—humanity. The human genome
evolutionary pop science. Today, Oxford Uni- everyone. The result, they say, is a “relax- project and genetic data from people around
versity geneticist Bryan Sykes is receiving ation” of the selective pressures that might the world have powered an explosion of
voluminous coverage for his book, Adam’s have operated 50 or 100 years ago. “Biolog- research seeking signs of natural selection
Curse, which predicts that continuing degen- ically, human beings are going nowhere,” in human DNA. “A lot of the tools we are
eration of genes on the Y chromosome will says anthropologist Ian Tattersall of the now using to search for selection were
leave men sterile or even extinct in 125,000 American Museum of Natural History in developed by people working on flies and
years. Many biologists say that the question New York City. University College London other organisms,” says evolutionary geneti-
they most often receive from students and the geneticist Steven Jones agrees. “The central cist Bruce Lahn of the University of
public is “Are humans still evolving?” issue is what one means by ‘evolving,’ ” Chicago. “But once researchers began to
To many researchers, the answer is obvi- Jones says. “Most people when they think discover examples of ongoing selection in
ous: Human biology, like that of all other liv- of evolution mean natural selection, a humans, it opened the door and gave them
ing organisms on Earth, is the result of natu- change to a different or better adapted state. confidence that they could find even more.”
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234 8 JULY 2005 VOL 309 SCIENCE www.sciencemag.org
Published by AAAS
 N E W S F O C U S

So far, the number of confirmed cases of regional differences in head shape—param-

genes under recent selective pressure is only eters such as width of the skull, height of the
“a handful,” says Tyler-Smith. But that is nose, and length of the jaw—to see whether
likely to change once the results of the Inter- certain traits were favored by natural selec-
national HapMap Project, a multination tion in response to differences in climate or
effort to determine worldwide variation in environment. In most cases, the differences
the human genome, are released later this among populations turned out to be no more
year. Because genetic variation is the raw than expected due to random drift. But there
material on which natural selection works, are a few exceptions: Anthropologist
favoring certain alleles over others, Tyler- Charles Roseman of Stanford University in
Smith says the HapMap should “give us an California last year reported in PNAS that
overall view of the regions of the genome the skulls of the Buriat people of Siberia are
that have been under selection.” broader than predicted by random drift.
Broad skulls have smaller surface areas and
Drifting toward modernity? so may be an adaptation to cold climates.
To science-fiction fans, the future of human That fits with previous work by anthropolo-
evolution conjures up visions of dramatic gist John Relethford of the State University
changes in our bodies, such as huge brains of New York College at Oneonta. Releth-
and skulls. “Many people see us continuing ford concludes that random drift and migra-
on the righteous path of increasing intelli- Cold adapted. Natural selection may have tion can explain cranial differences in “most
gence,” says Pavelka. “But we will not head favored the Buriats’ broad skulls. cases,” with the exception of people like the
in the direction of larger brains and crania as Buriat and Greenland Eskimos, who live in
long as infants are required to pass through concluded last December in the Proceed- very cold environments.
a woman’s pelvis to get into the world.” ings of the National Academy of Sciences Although the evolution of measurable
Whatever lies in our evolutionary future, (PNAS) that natural selection probably traits such as modern human skull shape may
scientists agree that the modern human drove the evolution of facial form up to the be due to random drift, some changes in
body form is largely the result of evolution- birth of early Homo. But they also found human body form may have more to do with
ary changes that can be traced back millions that genetic drift could explain most of the cultural and environmental factors such as
of years. The uniquely human lineage dates changes in the human face after the birth of diet. “Over the past 10,000 years, there has
from about 6 million years ago, and many Homo about 2.5 million years ago. “Selec- been a signif icant trend toward rounder
studies have demonstrated that our diver- tive pressures on the face may have been skulls and smaller, more gracile faces and
gence from chimpanzees was accompanied released” when humans began using tools jaws,” notes anthropologist Clark Larsen of
by strong selective pressure, for example on and so did less biting and chewing, says Ohio State University in Columbus. Most of
the human brain. Yet researchers caution Ackermann. the change, says Larsen, is probably due to
that not all morphological changes—the The take-home lesson, she says, is that how we use our jaws rather than genetic evo-
ones we can see in body shape and size “genetic drift has played an important role lution. With the rise of farming, humans
—are the result of natural selection; some in shaping human diversity. This is evolu- began to eat much softer food that was easier
may not be due to genetic evolution at all. tion, too.” Drift has continued to shape to chew. The resulting relaxation of stress on
For example, the increase in average height modern human faces and skulls in the more the face and jaw triggered changes in skull
seen in many developed nations over recent past, according to other studies. For shape, Larsen says. He adds that the dramatic
the past 150 years or so is probably due example, researchers have examined and worldwide increase in tooth maloc-
mostly to better diets rather than clusion, tooth crowding, and
natural selection. impacted molars are also signs of
Even very early evolutionary Candidates for Recent Selection in Humans these changes: Our teeth are too
changes in the hominid line were big for our smaller jaws. Numer-
GENE OR GENETIC LOCUS HYPOTHESIZED SELECTIVE PRESSURE
not necessarily due to natural ous studies show that non-West-
selection. Take the hominid face, Lactase Improved nutrition from milk ern people who eat harder tex-
which has changed dramatically tured foods have very low
in the past 3 million years from G6PD Protection against malaria rates of malocclusion, he
the heavy-jawed mugs of the aus- Duffly blood group Protection against malaria notes. Similar changes are
tralopithecines to the relatively found in monkeys fed hard
small and gracile skulls of mod- Hemoglobin C Protection against malaria and soft diets. “With the
ern humans. Anthropologist Protection against malaria reduction in masticatory
TNFSF5
CREDITS (TOP TO BOTTOM): GETTY IMAGES/AFP; IMAGE: CDC

Rebecca Ackermann of the Uni- stress, the chewing muscles

versity of Cape Town in South CCR5 Protection against smallpox and AIDS grow smaller, and thus the bone
Africa and anatomist James grows smaller,” Larsen says. “It is
H2 haplotype Unknown but only in Europe
Cheverud of the Washington not genetic but rather reflects the
University School of Medicine in DRD4 Cognition and behavior great plasticity of bone. It is a bio-
St. Louis, Missouri, analyzed logical change but heavily influ-
hominid faces over time, using MAOA Cognition and behavior
enced by culture.”
formulas that model natural AGT Protection against hypertension
selection as well as random Signs of selection
genetic drift, in which some traits CYP3A Protection against hypertension Even if random drift and other
or alleles become more common TAS2R38 Bitter taste perception nongenetic forces have helped
simply through chance. They shape modern humans, there is
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www.sciencemag.org SCIENCE VOL 309 8 JULY 2005 235
Published by AAAS
 N E W S F O C U S

but is absent in the Bantu of South Africa

and most Chinese populations. Hirschhorn
and colleagues concluded from the unusual
length of the DNA block that it is young,
because it has not yet been broken up by
genetic recombination. They calculate in
the June 2004 issue of the American Jour-
nal of Human Genetics that this haplotype
came under very strong selective pressure
beginning between 5000 and 10,000 years
ago, corresponding to the rise of dairy
farming. Thus a cultural and technological
change apparently fostered a genetic one.
“This is one of the best examples of recent
selection in humans,” says Tyler-Smith.
Although being able to drink milk as an
adult has its pleasant side, as any chocolate-
shake lover can testify, most people in the
world get along fine without the beverage. Yet
in some cases, having a certain allele can be a
matter of life or death. Thus, the genes most
likely to be under strong selective pressure
today are probably those involved in provid-
Battle for survival. AIDS and other deadly diseases may spur a rise in resistant gene alleles. ing resistance to infectious disease, says
Sarah Tishkoff, a geneticist at the University
growing evidence that natural selection has today. Some of these favored alleles appar- of Maryland, College Park. “In Africa, people
also played an important role, even if its ently arose at highly critical periods in human are dying daily [of infectious disease], and
effects have been more subtle. Human evolution. Such is the case of FOXP2, the so- those who have genotypes that confer some
evolution researchers are now mining the called speech gene, which is implicated in the resistance are going to have more offspring.
riches of genomic data to spot genes subject ability to talk, shows signs of strong selec- That is natural selection in action.”
to recent selective pressures (Science, tion, and arose no more than 200,000 years AIDS and malaria are arguably the worst
15 November 2002, p. 1324). Geneticists ago, coinciding closely with the first appear- scourges of humankind today, and they may
have a large arsenal of “tests of selection” at ance of Homo sapiens (Science, 16 August both be exerting selective pressure on
their disposal, all of which exploit the 2002, p. 1105). Other genes under selection African genomes. Several genes have alle-
genetic diversity of human populations to are linked to cognition and behavior, and still les that provide resistance to malaria,
determine whether individual alleles or others are involved in defense against dis- including those that code for hemoglobin C
larger blocks of the genome—called haplo- eases such as hypertension, malaria, and and an allele of the so-called Duffy blood
types—are behaving as would be expected AIDS (see table, p. 235). group found only in sub-Saharan Africa;
if they were only subject to random drift and In some cases, the new tests for selection accumulating evidence suggests that they
were not under selection. have helped nail down long-suspected cases have both been under recent selective
Some tests look for evidence that muta- of evolutionary adaptation. One classic pressure. Four years ago, Tishkoff and
tions in an allele that alter the protein it example is lactase persistence, the inverse colleagues showed that two different alleles
codes for have been favored over those that condition of so-called lactose intolerance. of a gene called glucose-6-phosphate
cause no change; others examine whether Most adults cannot drink milk because they dehydrogenase (G6PD) have also been
certain alleles are more common than produce little lactase, the enzyme that favored by strong selective pressure. The
expected. A fairly new and powerful breaks down lactose, which is the major mutant alleles, A– and Med, are found only
approach compares the frequency of an sugar in milk. But a sizable number of peo- where malaria is or recently was a problem
allele in a population with the genetic diver- ple can, and their geographical distribution and offer resistance against malaria,
sity within a haplotype to which it belongs. correlates closely with the spread of domes- although they can cause blood diseases.
If the allele is common due to random drift ticated cattle out of the Near East. Thus, Tishkoff and her co-workers used the
over a long time, the adjacent region of the more than 70% of Europeans, who have a long known geographical variations in the G6PD
genome should show considerable variation history of drinking milk, have lactase persist- gene to estimate that the A– allele probably
due to genetic recombination, the exchange ence, as do some African pastoralists. In con- arose in Africa about 6300 years ago and then
of DNA between chromosomes during mei- trast, the percentage is very low in most of spread rapidly across the continent; the Med
otic cell divisions. But if the variation is less sub-Saharan Africa and Southeast Asia. allele, found in southern Europe, the Middle
than expected, the allele may have risen to Last year, researchers clinched the case East, and India, is estimated to be only about
high frequency in a much shorter period of for selection at the lactase gene. A team led 3300 years old (Science, 20 July 2001,
time—a telltale sign of selection. “These by genome researcher Joel Hirschhorn of pp. 442 and 455). These estimates are consis-
tools are powerful,” says Lahn. “Where we Harvard Medical School in Boston identi- tent with archaeological evidence that
are lagging behind is in good data.” f ied a haplotype more than 1 million malaria only became a major health problem
CREDIT: ASSOCIATED PRESS

By deploying such methods, geneticists nucleotide base pairs long that includes the after the invention of farming, when the clear-
have identified more than two dozen genes lactase gene and confers lactase persistence ing of forests left standing pools of water in
that appear to have come under selective on people who carry it. This form of the which the vector for the disease, the Anophe-
pressures since the rise of Homo, and several haplotype is found in nearly 80% of Euro- les mosquito, could breed. Thus a cultural
of them may still be subject to such pressures peans and Americans of European ancestry change again led to a genetic one.
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Published by AAAS
 N E W S F O C U S

The case of AIDS, and the virus that dence for positive selection was stunning: rently acting on the human genome means
causes it, HIV, suggests that the selective As the team reported in the February 2005 that humans are still evolving, even if in
advantage of a gene can shift over time. As issue of Nature Genetics, female H2 carrierssubtle ways. But can we actually predict the
HIV infects T cells in the blood, it docks had about 3.5% more children than H1 car- course of future evolution, à la Sykes’s dis-
onto a cell surface receptor called CCR5. In riers. “This study has large implications,” appearing males or the vanishing blonds?
the mid-1990s researchers discovered that a says anthropologist Osbjorn Pearson of the Most researchers’ predictions are consider-
mutation in the CCR5 gene provides strong University of New Mexico, Albuquerque. ably more narrow and cautious and are tied
protection against AIDS in homozygotes, “The European version of the H2 haplotype to known selective pressures.
people who have two copies of the protec- could sweep the entire human population if For example, researchers predict that
tive allele. The mutation, called delta 32, is it conveyed the same reproductive advan- delta 32 and other protective CCR5 muta-
found in up to 13% of European popula- tage in other people and environments.” But tions may become more common in popula-
tions but is extremely rare in other groups, deCODE CEO and research team co-leader tions widely infected with HIV, especially
including Africans. Researchers dated the Kári Stefánsson says the low frequencies of in Africa. “If there are no more advances in
origins of the delta 32 mutation the treatment of AIDS and peo-
in humans to about 700 years ple continue to die, we would
ago and concluded that a strong expect selection pressure to
selective event resulted in its increase [the mutations’] fre-
spread; this f inding was con- quency over time,” says Tyler-
firmed in 2001 using sophisti- Smith, who adds that he sees “no
cated selection tests. reason why they should not go to
Yet because the AIDS epi- f ixation”—that is, replace all
demic dates only from the late other alleles of the gene.
1970s at the earliest, researchers Whether or not these patterns
believe that the selective pressure will make a significant differ-
on the delta 32 mutation must ence in the way humans look or
have been from some other live is another question. “There
factor. Researchers have debated will be minor fluctuations over
whether the plague or smallpox, time and space in the makeup of
both of which ravaged European local human gene pools as
populations in the past, is more humans respond to local condi-
likely, although some recent stud- tions,” predicts Tattersall, “but
ies have leaned toward smallpox. they won’t be directional. I find
it hard to foresee that under cur-
Icelanders evolving? rent conditions a qualitatively
Although researchers scouring new kind of human is ever likely
the human genome for signs of Baby boost. Women with an inversion in this region of chromosome 17 to emerge. But if conditions
natural selection have uncovered have more children. change, all bets are off.”
a few examples, direct evidence Evolutionary predictions are
that a particular allele actually boosts repro- H2 outside Europe suggest that for some tied to speculation about just what kind
duction—the sine qua non of natural selec- reason, its advantages are limited to that of environment we may face. Some
tion—is hard to come by in humans. But continent. “Why, I can’t tell you,” he says. researchers suggest that changing climate
that’s just what researchers were able to do in There are several genes in the H2 region, conditions may diminish the benefits of cul-
one dramatic study in Iceland. For the past but it is not at all clear which ones cause H2 ture and medicine, creating a new era of nat-
several years, scientists at deCODE Genet- carriers to have more children; one nearby ural selection. “There has been a relaxation
ics, a biotechnology company based in gene is implicated in pregnancy complica- in selective pressures in industrialized soci-
Reykjavik, Iceland, have been gathering tions. The deCODE team is looking at the eties,” says evolutionary geneticist Peter
genetic information on the nation’s 270,000 genes to see whether differences in expres- Keightley of the University of Edinburgh,
citizens, in a government-approved effort to sion might create the selective advantage. U.K. “But our ability to sustain that relax-
isolate disease genes (Science, 24 October One lead, Stefánsson says, is that H2 carri- ation is probably temporary. We are using
1997, p. 566). In the course of this research, ers also show a higher rate of recombination up our energy resources, our population is
deCODE researchers discovered a variant of during meiosis. In an earlier study, his team growing, and the climate is changing. All
human chromosome 17 in which a 900,000 - found that mothers with high oocyte recom- this is bound to lead to greater difficulties
nucleotide-base-pair stretch of DNA was bination rates also tend to have more chil- and renewed selective pressures.”
inverted; this inversion was associated with dren, possibly because this genetic shuf- Despite such concerns, however, most
a previously identified haplotype called H2, fling helps protect against errors in meiosis, scientists remain leery of long-term fore-
which they estimate arose 3 million years which are a major cause of miscarriage in casts, in part because of the way evolution
CREDIT: NATURE GENETICS 37, 129-137 (2005)

ago. H2 carriers make up about 17.5% of older mothers. H2 carriers also appear to works. “Evolution is not directed towards a
Icelanders and 21% of Europeans, but only live longer on average. “It is fascinating to goal,” says Tyler-Smith. “It always takes the
about 6% of Africans and 1% of Asians. think that there might be an advantage asso- short-term view, operating just on what
To see whether the relatively high fre- ciated with a DNA variant at both ends of allows us to survive and reproduce better in
quencies in Europeans represented natural life,” Stefánsson says. this generation.” For now, predicting
selection, the team genotyped 29,137 Ice- humanity’s evolutionary future may be little
landers born between 1925 and 1965. When Our evolutionary future more than crystal ball gazing—better suited
these data were correlated with the island’s To many researchers, the limited but grow- to science fiction than scientific research.
extensive genealogical database, the evi- ing evidence that natural selection is cur- –MICHAEL BALTER
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www.sciencemag.org SCIENCE VOL 309 8 JULY 2005 237
Published by AAAS
EJERCICIOS
DE

REPASO

268
269
Problema 1.
El Dr. H. estudia dos “variedades” de angiospermas (plantas con flores) que
habitan en una pradera y un bosque de una misma región geográfica. A lo
largo de varios años ha colectado la siguiente información:
i) En el año 2006 el investigador realizó un estudio con plantas de la
pradera y del bosque analizando los caracteres: largo del tallo,
número de hojas, concentración de carotenos en las flores, largo de
los estambres y número de estomas por cm3. Combinó toda esta
información en dos variables nuevas y obtuvo el siguiente gráfico:

ii) En el año 2007, realizó cruzamientos de plantas de ambas

poblaciones cortando los estambres de las flores y fecundando las
mismas artificialmente en el laboratorio. Sembró las semillas
producidas en el invernadero y obtuvo los siguientes resultados:
Flores pradera x polen pradera: 200 plantas
Flores pradera x polen bosque: 150 plantas
Flores bosque x polen bosque: 150 plantas
Flores bosque x polen pradera: 185 plantas
iii) Al año siguiente decidió transplantar individuos a los que les había
cortado los estambres desde la población del bosque a la pradera y
viceversa. Cuando analizó la cantidad de semillas en las flores de cada
población, encontró los siguientes valores promedio:

Pradera:
Individuos originarios de la pradera: 5 ± 1 semillas/flor
Individuos originarios del bosque: 0,2 ± 0,1 semillas/flor

Bosque:
Individuos originarios de la pradera: 1 ± 0,2 semillas/flor
Individuos originarios del bosque: 20 ± 4 semillas/flor

270
a. Interprete la información de los tres estudios y explique los resultados
obtenidos.
b. Especifique cuántas especies podrían definirse para estas dos variedades de
angiospermas de acuerdo a los conceptos de especie morfológico, ecológico,
biológico y cohesivo. Justifique claramente sus respuestas.
c. Para el concepto de especie que corresponda, indique el/los mecanismo/s de
aislamiento reproductivo existentes.
d. ¿En cuál de las dos escuelas teóricas sobre el proceso de especiación
(aislacionista o seleccionista) cree Ud. que se encuadra el trabajo del Dr. H.?
Justifique.
e. Compare ambas escuelas con respecto a: el concepto de especie utilizado,
cuáles serían los “genes de especiación”, el papel de la selección natural y la
deriva génica en el proceso especiogénico y el modelo geográfico
paradigmático.

Problema 2.
En Drosophila, como en todos los insectos holometábolos, el crecimiento
corporal está restringido a los estadios larvales. Las larvas se alimentan y
crecen exponencialmente hasta alcanzar un tamaño crítico que se alcanza al
comienzo del tercer estadio larval. En este momento se inicia una cascada
hormonal que desencadena en la liberación de ecdisteroides. Un primer pico de
liberación de ecdicteroides produce que la larva deje de alimentarse y busque
un lugar para comenzar la metamorfosis. Al dejar de comer, la larva detiene su
crecimiento corporal alcanzando el tamaño corporal final (los adultos tienen un
exoesqueleto que impide posteriores incrementos en el tamaño del cuerpo).
Existe una separación temporal entre el momento en que la larva deja de
alimentarse y el momento en que se alcanza el tamaño corporal final. Este
periodo se conoce como periodo de crecimiento terminal (TGP).
En los insectos holometábolos, los órganos (como por ejemplo, las alas) se
originan como discos imaginales dentro de la larva. Como en el caso del
crecimiento corporal, los discos imaginales también crecen exponencialmente
dentro de las larvas hasta diferenciarse en órganos adultos. La finalización del
crecimiento parece estar regulada por la misma cascada hormonal que regula
el crecimiento del cuerpo.
Ud. está interesado en estudiar el desarrollo ontogenético de las alas en un
grupo de especies de Drosophila que presenta variabilidad para el tamaño de
las mismas. En la figura 1 se muestran las relaciones filogenéticas entre las
especies utilizadas en este estudio (fig. 1.a) y los resultados obtenidos al
analizar la relación entre la superficie del cuerpo (tomado como superficie del
tórax) y el área de las alas (fig. 1.b):

271
(a) (b)
C (círculos)

A (triángulos)

B (cuadrados)

Figura 1.
(a) Relaciones filogenéticas entre
las especies estudiadas. (b) Relación
entre la superficie del cuerpo
y el área de las alas.

En la figura 2 se muestran los resultados del estudio de diferentes parámetros

del desarrollo de las alas (disco imaginal – órgano) y el cuerpo para este grupo.

Figura 2: L1, L2 y L3 son estadios larvales. La escala de tiempo es la misma para las
especies a, b y c. El grafico de la izquierda corresponde a las especies a y c. El grafico
de la derecha a la especie b.

a. Defina los términos alometría evolutiva y alometría ontogenética e

identifique un ejemplo de cada una en el caso de estudio.
b. Teniendo en cuenta los datos de la figura 2, ¿Es sincrónica la finalización del
desarrollo del cuerpo y de las alas en la especie a? ¿Y en la especie b?
Justifique.

272
c. Para las especies a y b: ¿son homólogos los estadios larvales tres días
después de la eclosión del huevo (flechas negras gruesas en el eje tiempo)?
¿Se podrían usar estos individuos para estudiar comparativamente los patrones
de crecimiento alométricos entre ambas especies? Justifique todas sus
respuestas.

d. Teniendo en cuenta todos los resultados aquí expuestos, indique si las

siguientes afirmaciones son verdaderas o falsas. Justifique brevemente las
falsas.
d.1. El reducido tamaño de las alas y del cuerpo en los adultos de la especie
b (con respecto a los adultos de las especies a y c) podría explicarse porque
el tamaño crítico se alcanza a menor tamaño corporal durante la ontogenia
de b.
d.2. El reducido tamaño de las alas y del cuerpo en los adultos de la especie
b (con respecto a los adultos de las especies a y c) podría explicarse porque,
una vez alcanzado el tamaño crítico, la tasa de crecimiento de los discos
imaginales en la especie b es más lento.
d.3. El reducido tamaño de las alas y del cuerpo en los adultos de la especie
b (con respecto a los adultos de las especies a y c) podría explicarse por un
acortamiento del periodo de crecimiento terminal de los discos imaginales
de la especie b.

Problema 3:

Lea cuidadosamente el siguiente párrafo y responda las preguntas a

continuación:

“El paleontólogo alemán A. Seilacher ha puesto de manifiesto estos

últimos años la existencia de motivos arquitectónicos en las conchas de
moluscos y braquiópodos. Existe en estos animales un modo
arquitectónico denominado modo divaricado. Se trata de una estructura
en líneas divergentes (o en cabríos) ya sea en las líneas de ornamentación
de las conchas (costillas) o, en los motivos coloreados, en la
mineralización de las estructuras internas o, en fin, en la forma de las
ranuras. Seilacher estima que en la mayoría de los casos no hay buenas
razones para que las costillas, coloraciones, etc. tengan una estructura
divergente. Por ejemplo, los modos de coloración en cabríos no pueden
tener utilidad (como, por ejemplo, dispositivo de camuflaje visual frente a
los predadores) ya que las pechinas que lo presentan viven enterradas en
la arena, donde además están recubiertas por el perióstracum que
enmascara la coloración de la concha. Seilacher considera que las
estructuras divergentes comunes de moluscos y braquiópodos son
expresión de un modo arquitectónico divaricado, el cual podría proceder
de ciertas inhomogeneidades en el manto de crecimiento, probablemente
en función de la producción de figuras de interferencia alrededor de los
centros dispuestos regularmente (algunas simulaciones simples por
ordenador pueden generar estas formas).”

273
a. ¿Qué mirada macroevolutiva (A, B, ambas o ninguna) subyace a este
escenario particular? Justifique su respuesta.
b. ¿Qué otros elementos o procesos son característicos de dicha mirada?
Mencione al menos tres.
c. Describa sintéticamente dos debates actuales en torno a la macroevolución
especificando en qué consiste cada uno de ellos y las distintas propuestas que
encierran. (Nota: para esto se sugiere revisar el artículo de S. J. Gould (1983)
estudiado en el bloque de macroevolución).

Problema 4.
Los piojos son insectos parásitos obligados de mamíferos y aves y por ende,
poseen aspectos de su ecología e historia evolutiva íntimamente ligados a los
de sus hospedadores. Su transmisión se produce por contacto directo entre sus
posibles hospedadores y su ciclo de vida se desarrolla completamente sobre el
cuerpo de los mismos.
a. Correlacione cada una de las siguientes figuras con un modelo geográfico de
especiación para los organismos parásitos. Justifique se respuesta.

G: área geográfica. H: hospedador. Punto negro: parásito.

En el caso particular de los piojos de los primates, los mismos son especie
específicos y esta alta especificidad es la que permite la detección de patrones
coevolutivos. Los humanos son parasitados por dos especies de piojos: Pthirus
pubis, que vive en el pubis y Pediculus humanus que tiene dos variantes
morfológicamente similares pero ecológicamente diferentes. Una vive en la
vestimenta, se desplaza hasta el cuerpo para alimentarse una o dos veces por
día y es vector de la bacteria que produce el tifus. A esta variante se la llama
piojo del cuerpo. La otra vive en la cabeza, se alimenta con mayor frecuencia y
no es vector de ningún agente patogénico.
La Figura 1, muestra la filogenia de los piojos de los primates y la de sus
hospedadores y la Figura 2, la distribución actual de los simios antropomorfos
africanos y de los fósiles más antiguos de australopitecinos.

274
Figura 1. Filogenia de los primates y de sus respectivos piojos. OW monkeys: monos
del Viejo Mundo (macacos y babuinos).

Figura 2. Distribución actual de los simios

antropomorfos africanos. Círculos negros: lugares
donde se encontraron los fósiles más antiguos de
australopitecinos.

275
b. A partir de esta información, proponga un modelo geográfico de especiación
para los piojos de los géneros Phtirus y Pediculus. Explique mediante el mismo
cómo pudo producirse la divergencia entre los dos géneros y entre las especies
dentro de los géneros, sin olvidar mencionar si en algún caso pudo haberse
producido un salto de hospedador.
Un análisis filogenético basado en los genes mitocondriales Cyt b y COI de las
variantes del cuerpo y de la cabeza de P. humanus mostró el siguiente
cladograma:

Figura 3. El tamaño de los triángulos es proporcional a la cantidad de linajes

comprendido por el clado.

Un análisis del D de Tajima mostró desvíos significativos de la neutralidad y

consistentes con una expansión poblacional reciente (entre 0,5 y 0,1 millones
de años, según datos de reloj molecular) sólo en el clado A.
c. Según los conceptos morfológico, ecológico y cladístico, ¿pueden
considerarse las variantes de P. humanus de la cabeza y del cuerpo especies
distintas?
d. Dado que los parásitos pueden usarse para hacer inferencias sobre la
historia evolutiva de sus hospedadores, ¿qué modelo de evolución del hombre
moderno avala estos dos últimos análisis? ¿Qué sugieren respecto de la
interacción de Homo sapiens con otros linajes de homininos?

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Problema 5.
Un grupo de investigación se ha dedicado durante años a estudiar un conjunto
de coleópteros que comparten varias sinapomorfías. Las 15 especies
analizadas, como la mayoría de las pertenecientes al mismo orden, poseen dos
pares de alas: un primer par coriáceo (élitros) en el segundo segmento del
tórax, y un segundo par membranoso en el tercer segmento del tórax.
Después de realizar muchos experimentos, los investigadores llegaron a la
conclusión de que el desarrollo de dichos apéndices está controlado por una
serie de genes que interactúan entre si, que prácticamente no muestra
diferencias entre las especies estudiadas.
a. ¿Puede identificar alguna/s homología/s en el caso de estudio? ¿De qué tipo?
Justifique.
Posteriormente, la investigación se centró en un par de especies hermanas (A y
B). Los investigadores obtuvieron estimaciones del tamaño de ambos pares de
alas y del tamaño corporal total, y concluyeron que las especies analizadas
sólo difieren respecto del tamaño de los élitros. Determinaron que la especie A,
que posee un primer par de alas más grande, muestra una tasa de
proliferación celular mayor en el tejido a partir del cual se genera ese par de
alas durante la metamorfosis.
b. ¿A qué tipo de alometría se refieren estos resultados?
c. ¿Qué fenómeno podría explicar dichos resultados? ¿Qué observaciones
confirmarían su hipótesis?
Dado que las especies mencionadas previamente fueron mantenidas en el
laboratorio durante muchos años, los investigadores pudieron observar la
aparición de ciertos mutantes. Particularmente, la aparición de un segundo par
de élitros en lugar del par de alas membranosas. Cuando los investigadores
obtuvieron nuevas muestras de poblaciones naturales no hallaron ningún
individuo que mostrara el fenotipo obtenido en el laboratorio.
d. ¿Cómo podría explicar estos resultados? Justifique.

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Problema 6.
En la figura a continuación se observan los rangos de volumen cerebral que
presentan diferentes géneros de homínidos a lo largo del tiempo.

Sabiendo que dentro de cada intervalo y género puede haber más de una
especie morfológica:
a. Redacte un breve párrafo explicando el patrón observado utilizando
elementos típicos de una “mirada A” o “el mejor de los mundos posibles”. Sea
conciso y argumente claramente en no más de 15 renglones.
b. Explique el mismo patrón utilizando elementos y procesos típicos de una
“mirada B” o “un mero mundo posible”. Sea conciso y argumente claramente
en no más de 15 renglones.
NOTA IMPORTANTE: Se evalúa el contrapunto entre los tipos de mirada y NO su
conocimiento sobre el tema de encefalización en particular.

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Problema 7.
Empleando el esquema de relaciones del linaje homínido de Tattersall 2005:
a. ¿Considera Ud. que dicho esquema avala el modelo de evolución propuesto
por los defensores de Eva mitocondrial? Justifique su respuesta
b. Utilice 5 fósiles de este esquema para proponer una hipótesis alternativa
sobre evolución de los homínidos seleccionando del siguiente listado los
términos que considere adecuados para incluir en su relato:
coexistencia de varias especies / hipótesis de la especie única / cambio
gradual / procesos contingentes / adaptación al ambiente / cooptación de
cuerdas vocales / procesos microevolutivos / grupos hermanos / selección
de especies.
c. Indique dos críticas realizadas al modelo de Eva mitocondrial por parte de
los defensores del modelo Multirregional de evolución humana y viceversa.
d. Indique qué hipótesis de evolución del hombre moderno apoyaría cada uno
de los siguientes hallazgos. Justifique brevemente
d.1) Restos fósiles con características anatómicas modernas de
aproximadamente 300000 años hallados en África.
d.2) Los restos fósiles de hombres arcaicos hallados en Asia exhiben las
características típicas de las poblaciones actuales.
d.3) La estimación del origen del HSAM utilizando secuencias del
cromosoma Y fue de 190.000 años.

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Problema 8.
Ud. es un referente a nivel internacional de la escuela seleccionista de
especiación. En particular, supone que la especiación en clados como el de los
mamíferos se produce principalmente en simpatría.
Recientemente comenzó a trabajar en colaboración con paleoantropólogos con
el objetivo de indagar los mecanismos subyacentes a las radiaciones
especiogénicas observadas en el registro fósil del linaje humano. Una primera
instancia de este proyecto consiste en reconstruir el proceso responsable de la
diversificación dentro del grupo de los australopitecinos africanos.
a. Utilizando los supuestos del modelo de especiación en simpatría y sus
conocimientos sobre las diferencias morfológicas existentes entre
australopitecinos gráciles* y australopitecinos robustos**, proponga un
escenario de especiación para explicar el surgimiento de ambos morfos en
África.
Organice su respuesta en torno a los siguientes ejes:
- distribución geográfica de la especie ancestral;
- características del ambiente;
- período geológico en el que ocurrió la divergencia;
- mecanismo evolutivo responsable de la divergencia;
- genes de la especiación;
- distribución geográfica de los morfos descendientes;
- resultado/s del proceso.
* Australopitecinos gráciles: grupo que incluye a las especies Australopithecus
anamensis, Australopithecus afarensis, Australopithecus africanus entre otros.
** Australopitecinos robustos: grupo que incluye a las especies Paranthropus
boisei, Paranthropus robustus; Paranthropus aethiopicus entre otros.

b. ¿Qué concepto de especie es utilizado para definir a las especies de

australopitecinos? ¿Y para reconstruir este escenario de especiación?

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