Diformism Sexual
Diformism Sexual
Diformism Sexual
ABSTRACT Sexual dimorphism is a pervasive phe- ontogenetic pathways that can lead to dimorphism, and
nomenon among anthropoid primates. Comparative anal- provide additional insight into the selective mechanisms
yses over the past 30 years have greatly expanded our that influence dimorphism throughout the lifetime of an
understanding of both variation in the expression of di- animal. Evidence from the fossil record suggests that di-
morphism among primates, and the underlying causes of morphism probably evolved in parallel twice, and the di-
sexual dimorphism. Dimorphism in body mass and canine morphism in some extinct hominoids probably exceeded
tooth size is familiar, as is pelage and sex skin dimor- that of any living primate. Our advances in understanding
phism. More recent analyses are documenting subtle dif- the behavioral/ecological correlates of dimorphism in liv-
ferences in the pattern of skeletal dimorphism among ing primates have not improved our ability to reconstruct
primates. Comparative analyses have corroborated the
social systems in extinct species on the basis of dimor-
sexual selection hypotheses, and have provided a more
phism alone, beyond the inference of polygyny or intense
detailed understanding of the relationship between sexual
selection, natural selection, and mating systems in pri- male-male competition. However, our understanding of
mates. A clearer picture is emerging of the relative con- the behavioral/ecological correlates of growth and devel-
tribution of various selective and nonselective mecha- opment, and of the expression of dimorphism as a function
nisms in the evolution and expression of dimorphism. of separate changes in male and female traits, offers great
Most importantly, recent studies have shown that dimor- potential for inferring evolutionary changes in behavior
phism is the product of changes in both male and female over time.Yrbk Phys Anthropol 44:2553, 2001.
traits. Developmental studies demonstrate the variety of 2001 Wiley-Liss, Inc.
TABLE OF CONTENTS
Sexual dimorphism is a common phenomenon sex differences. Primary sex differences are those
among living and extinct primates. The past several directly related to mating and reproduction, includ-
decades have seen a steady growth in studies of ing obstetrically related differences in the pelvis.
dimorphism, ranging from simple documentation of Secondary sex differences are any other differences
the phenomenon in various species to broad compar- not directly related to mating. Primary sex differ-
ative analyses incorporating humans and a wide ences are not often referred to as dimorphic char-
variety of primates. Consequently, our understand- acters (though there is nothing wrong with doing
ing of the expression, evolution, and development of so). Rather, the term sexual dimorphism is usually
sexual dimorphism in primates and humans has reserved for secondary sex differences, particularly
increased dramatically. if they are thought to arise from sexual selection
This essay reviews recent advances in our under- (Crook, 1972). However, the term is sometimes used
standing of the expression and evolution of dimor- with reference to any sexual difference, including
phism across primates. However, it should be kept genetic and biochemical differences. For example,
in mind that anthropologists and primatologists are platyrrhine monkeys have sexually dimorphic al-
interested in sexual dimorphism for a variety of leles for color vision (Jacobs, 1994), while Gustafs-
reasons. Forensic anthropologists seek characters son (1994) discusses metabolic liver dimorphism in
that allow accurate sex identification on the basis of rats.
skeletal and dental remains. Human biologists are
Primary sex differences
interested in sexual dimorphism as a component of
population variation, and what it reveals about Primary sex differences are not commonly consid-
health and epiphenomenal adaptation in local pop- ered in discussions of the evolution of primate sex-
ulations. Systematists, morphologists, and paleon- ual dimorphism, but it is worth noting that the
tologists need to understand sexual dimorphism as a genitalia of primates can differ substantially in form
component of trait variation, either as a species- among species (Hershkovitz, 1977; Fooden, 1980;
specific character, or as a component of variation Dixson, 1987; Harcourt and Gardiner, 1994; Har-
that needs to be distinguished from potential inter- court, 1995; Verrell, 1992). For example, most male
specific character variation. Dimorphism can also primates have a bone (the baculum) in the penis
offer evidence about the behavior of extinct species. which differs in form and size among species. The
Primate biologists are interested in understanding baculum is lacking in Ateles, Lagothrix, Brachyteles,
the causes of sexual dimorphism in primates, and Chiropotes, Tarsier, and Homo (Hershkovitz, 1977).
how these relate to variation in behavior and ecology Penile morphology is highly variable (Hershkovitz,
(e.g., Crook, 1972; Leutenegger and Kelly, 1977; Ox- 1977; Harcourt and Gardiner, 1994; Harcourt,
nard, 1987; Plavcan and van Schaik, 1994; Leigh 1995). Generally, strepsirrhines tend to have spines
and Shea, 1995). on the penis, while most anthropoids do not (Har-
Most comparative analyses address two basic ques- court and Gardiner, 1994). Within these groups,
tions: what are the differences and similarities in the though, even closely related species can differ sub-
ways that dimorphism is expressed among species, stantially in penile morphology. Scrotal morphology
and what are the causes of variation in the magnitude is also variable, but to a lesser degree than penile
and pattern of dimorphism among species? In this morphology. Relative testicular volume also varies
essay, I review recent advances in answering these among species (Harcourt, 1995), as does the size of
two questions. I shall first survey dimorphism among the seminal vesicles (Dixson, 1997).
primates, focusing particularly on variation in the ex- There is also a wide variation in the external
pression of dimorphism. Next, I shall evaluate compar- appearance of the female genitalia: the labial folds,
ative models of the causes of sexual dimorphism in clitoris, and associated structures, even among
primates, including a discussion of sexual selection closely related species (Le Gros Clark, 1971; Hersh-
and behavioral ecological models of dimorphism, and kovitz, 1977). Additionally, the skin in and around
the relation between life-history, ontogeny, and dimor- the genital area varies widely among primates in
phism. Finally, I provide a brief survey of dimorphism cyclical changes associated with the menstrual cycle
in the fossil record and discuss whether it can be used (though this is usually considered a secondary sex
to reconstruct behavior. characteristic). Such sex-skins have evolved at
least three times among catarrhine primates, and
VARIATION IN DIMORPHISM IN PRIMATES are found in species of Pan, Colobus, Procolobus,
Definitions Papio, Macaca, Cercocebus, Lophocebus, Mandril-
lus, Theropithecus (swellings located on the chest),
Biologists recognize two basic types of dimorphic Miopithecus, and Allenopithecus. (Crook, 1972; Pa-
characters: primary sex differences and secondary gel, 1994; van Schaik et al., 1999; Nunn, 1999).
J.M. Plavcan] DIMORPHISM IN PRIMATES 27
These vary among species in size, shape, and dura-
tion.
The reasons for most interspecific variation in
genital morphology are unclear (Harcourt and
Gardiner, 1994; Harcourt, 1995). Sexual selection,
the common explanation for sexual dimorphism in
primates, probably plays little role in most variation
of the scrotum, penis, baculum, clitoris, labia, and
associated structures (Harcourt and Gardiner, 1994;
Harcourt, 1995). Some genital differences are
thought to function as a reproductive isolating
mechanism: variation in genital morphology can cre-
ate a lock-and-key morphology discouraging
closely related species from interbreeding. Such spe-
cies-specific variation can be useful for alpha taxon-
omy (e.g., Fooden, 1980). However, Le Gros Clark
(1971) notes that genital variation is so great, even
among closely related species, as to be useless for
higher taxonomic studies. There has been a great
deal of discussion of the evolutionary mechanisms
underlying variation in testicular volume (Dixson,
1987; Verrell, 1992; Harcourt, 1995), and in the ex-
aggerated perineal swellings of female catarrhines
(Harcourt, 1995; van Schaik et al., 1999; Nunn,
1999; Stallmann and Froehlich, 2000). These are
discussed below in the section on sexual selection.
Secondary sex differences Fig. 1. Illustration of lateral views of male and female Ma-
caca fascicularis skulls. This species shows typical dimorphism
Secondary sex differences are highly variable in for a cercopithecoid primate. Note magnitude of size difference
expression among primates, and are sometimes between male and female skulls, somewhat greater robusticity of
spectacular. For the most part, secondary sex differ- the skull, longer male face, and much larger male canine.
ence are confined to the anthropoid primates; strep-
sirrhine primates and tarsiers are, with a few excep- Reverse dimorphism 1 is only characteristic of
tions, monomorphic. The most obvious secondary some callitrichine primates and possibly some strep-
sex differences among primates are body mass di- sirrhines (Kappeler, 1990, 1991; Godfrey et al.,
morphism, and canine tooth size dimorphism. Skel- 1993; Plavcan and van Schaik, 1997b). In general,
etal dimorphism is often pronounced in primates, body mass dimorphism reaches its extremes in
and is primarily a product of body mass dimorphism hominoids and papionines. Platyrrhines on the
(Fig. 1). Pelage dimorphism, while not pervasive whole are characterized by lesser degrees of body
among primates, is present in several species and mass dimorphism, though there are a few species
can be quite impressive. Table 1 summarizes the (howler monkeys) that are comparable to cercopithe-
distribution of dimorphism among primates. coids (Ford, 1994; Plavcan and van Schaik, 1997b).
Body mass dimorphism. In most anthropoid pri- The canine/premolar complex. Canine tooth
mates, males are larger than females. The most size dimorphism is also common in anthropoids
extremely size-dimorphic primates are gorillas, or- (Crook, 1972; Leutenegger and Kelly, 1977; Harvey
angutans, mandrills, baboons, and proboscis mon- et al., 1978; Plavcan and van Schaik, 1992, 1994).
keys, with males sometimes more than twice as The maxillary canine teeth tend to be more dimor-
large as females (Crook, 1972; Clutton-Brock et al., phic than the mandibular canines. Cercopithecoid
1977; Leutenegger and Kelly, 1977; Plavcan and van male canine teeth tend to be very long and dagger-
Schaik, 1997b; Smith and Jungers, 1997). Most cer- like, and can be up to 400% taller than those of
copithecoid male primates range from about 30
80% larger than females in body mass. Body mass 1
The term reverse dimorphism is used to indicate that females are
differences between males and females are often larger than males. Some object to this term as sexist, reflecting male
characterized as species-specific traits, but there is bias in primatology. However, in primates almost all species have
good evidence for biologically meaningful subspecific males larger than females. Dimorphism is usually expressed quanti-
tatively as a ratio of the larger sex to the smaller (the opposite practice
variation in body mass dimorphism in some species is statistically inadvisable), meaning that ratios reflect male values
(Turner et al., 1994, 1997; Smith and Jungers, 1997; divided by female values. Reverse dimorphism is used to indicate that
Plavcan and van Schaik, 1997b; Jones et al., 2000). the opposite relation is true.
TABLE 1. Summary of body mass, canine tooth size, and pelage dimorphism in primates1
Taxon Body mass dimorphism Canine dimorphism Pelage and other dimorphisms
1
Anthropoid body mass from Plavcan and van Schaik (1997b). Strepsirrhine body mass dimorphism from Kappeler (1990). Anthropoid
canine dimorphism from Plavcan and van Schaik (1992). Strepsirrhine canine dimorphism from Kappeler (1991). Information on
pelage and other dimorphisms from Hershkovitz (1977), van Schaik et al. (1999), Crook (1972), and Fleagle (1999).
J.M. Plavcan] DIMORPHISM IN PRIMATES 29
surface of the tooth onto the root (Crook, 1972;
Fleagle, 1999). This gives the tooth a heart-shaped
occlusal outline which is easily recognized, espe-
cially in cercopithecoids.
While most female anthropoids have smaller ca-
nine teeth than males, their canines nevertheless
can be quite large (Plavcan and van Schaik, 1994;
Plavcan et al., 1995). Female canine tooth size
ranges from small, as in most colobines, to as large
as those of males, as in the hylobatids. Females of
some species also have a mesial groove, though not
as exaggerated as that of males. Importantly, canine
tooth size dimorphism is as much a function of vari-
ation in female canine tooth size as male canine
tooth size. For example, both Callicebus and Hylo-
bates show nearly monomorphic canine teeth. In
Callicebus, canines in both sexes are relatively short
and blunt, while in Hylobates, they are relatively
tall.
The mandibular premolar that lies adjacent to the
mandibular canine (P2 in platyrrhines and P3 in
catarrhines) can also be highly dimorphic (Zingeser,
1969; Crook, 1972; Greenfield, 1992a,b, 1996;
Greenfield and Washburn, 1992). In most species,
the male tooth is elongated to form a hone for
sharpening the back edge of the maxillary canine
tooth (Fig. 3). Consequently, the mandibular premo-
lar is often considered with the canines as part of the
canine/premolar complex. Females also can have
Fig. 2. Occlusal views of maxillary canine teeth of five pri-
mates, illustrating variation in canine size and shape among
an elongated premolar. Greenfield (1996) offers evi-
species, and within sexes. All teeth are oriented in same direc- dence that the hone of the female mandibular pre-
tion, with mesial at top, distal at bottom, lingual to left, and molar is overdeveloped by comparison to the size of
buchal to right. Note especially progression from strongly com- the maxillary canine. He proposes that the develop-
pressed in Varecia to rounded in Pongo, the heart-shaped outline ment of the female hone is a genetic correlated-
of male Macaca and Presbytis teeth associated with a deeply
excavated mesial groove, and differences in shape between males response to the development of the male honing
and females of Macaca and Presbytis. tooth. However, female canine crown height is
strongly correlated with female honing premolar
length, suggesting that the hone is functional in
females. Among anthropoids, male canines vary in females as well as in males (though this does not
size and shape (Fig. 2), ranging from fat, relatively rule out the effect of correlated response).
short teeth in the great apes (by comparison to cer-
copithecoids), to long, tall thin teeth in hylobatids Dental and skeletal dimorphism. Primates also
(Greenfield and Washburn, 1991; Greenfield, 1992a; show sexual dimorphism in the skeleton and teeth.
Plavcan, 1993a). Dimorphism is usually much Linear dimensions of the noncanine teeth can be up
greater in the crown height of the tooth than in the to about 10% larger in males than females (Garn et
occlusal dimensions (the measurements of length al., 1966; Plavcan, 1990; Cochard, 1985). It has been
and breadth at the base of the tooth). There are suggested that there is a field effect of sexual di-
distinctive patterns of canine dimorphism that cor- morphism in the dentition, centered on the canine
respond roughly to differences in male canine shape. teeth, such that teeth closer to the canines tend to be
Cercopithecoids tend to show proportionally greater more dimorphic than those farther away (Garn et
crown height dimorphism as compared to occlusal al., 1966). Others have suggested that different taxa
dimorphism, while in hominoids dimorphism tends share different patterns of sexual dimorphism in the
to be more uniform among the tooth dimensions. teeth (Lieberman et al., 1985; Oxnard, 1987). It ap-
Male and female canines in many species cannot pears, however, that noncanine tooth size dimor-
be easily sorted when they are similar in size. How- phism is largely a correlate of body mass dimor-
ever, Kelley (1995a,b) demonstrated that hominoid phism (Cochard, 1985; Wood et al., 1991). While the
male and female canine teeth can be sorted on the pattern of tooth size dimorphism in the dentition
basis of a few simple proportional differences, even tends to follow classic fields of tooth size, there are
where they do not differ substantially in size. Many no substantial, taxonomically significant patterns of
male anthropoid canines are characterized by a dimorphism in teeth other than the canines (Plav-
strong mesial groove running down the anterior can, unpublished findings).
30 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
At the very least, the results of all of these studies ary roles. Several papers expressed the opinion that
have led to a general recognition that dimorphism is sexual selection plays a minor, if any, role in ex-
multifactorial in expression and cause, following the plaining variation in dimorphism among living pri-
suggestion of Oxnard (1987). While there is little mate species (Lucas, 1981; Phillips-Conroy and
doubt now that sexual dimorphism is not a single Jolly, 1981; Rowell and Chism, 1986).
character, and that there are multiple factors that
affect its evolution and expression (Table 2), it has Recent models of mate competition, intrasexual
not been clear which factors are most important in competition, and dimorphism. A series of pa-
the evolution of dimorphism, and which play second- pers since the late 1980s reevaluated the sexual
J.M. Plavcan] DIMORPHISM IN PRIMATES 37
selection hypothesis, focusing on the problem of how 1992) and body mass (Plavcan and van Schaik,
to measure sexual selection. Early studies acknowl- 1997b) were significantly associated with compe-
edged the potential shortcomings of mating system tition levels, and with the separate intensity and
and socionomic sex ratio as measures of sexual se- frequency classifications. More importantly, the
lection (Clutton-Brock et al., 1977; Harvey et al., relationship between competition levels and di-
1978). To measure sexual selection, one should ide- morphism held within dietary categories, within
ally obtain accurate data on male reproductive suc- substrate classifications, and within a variety of
cess over time, coupled with information on male taxonomic groups. This strongly suggested that
intrasexual competition that directly leads to such sexual selection plays an important role in the
differential reproductive success. To test the hypoth- evolution of sexual dimorphism, regardless of the
esis that any particular character evolves as a con- effect of any other factor.
sequence of sexual selection, one needs data on Close examination of competition levels helps to
whether the character actually plays a role in the explain the poor correlation between mating system
outcome of competitive bouts that result in differen- classifications and dimorphism found in earlier
tial male reproductive success, and whether the studies (cf. Harvey et al., 1978; Leutenegger and
morphology of the character follows a predicted di- Cheverud, 1982, 1985; Cheverud et al., 1985; Phil-
rection. In short, one needs to show that bigger lips-Conroy and Jolly, 1981; Rowell and Chism,
males with bigger canines win more fights against 1986). Competition levels 2 4 all contain multimale/
other males, and as a result that they sire more multifemale species, but they make distinctions be-
offspring. Such data are not available for the over- tween the quality of male-male competition among
whelming majority of species. Hence, all tests of the different multimale breeding systems. For example,
sexual selection hypothesis use surrogate measures chimpanzee males (competition level 2) are known
of sexual selection that are derived from behavioral to show some agonistic competition, but in general
and demographic data that are assumed to reflect males are characterized by tolerant relationships
the strength of sexual selection (Mitani et al., 1996; with one another. By contrast, Saimiri males (com-
Plavcan, 1999). This issue is critical in any attempt petition level 3) live together in multimale groups
to claim that one factor is more or less important year round, but only form agonistic dominance hier-
than another in the evolution of sexual dimorphism.
archies during the breeding season. Theropithecus
How can we assert that body size is more important
males (competition level 4) form single-male har-
than sexual selection in the evolution of dimorphism
ems, but these aggregate daily into large groups
if our measure of sexual selection does not measure
where males come into close proximity with one
sexual selection?
another.
Kay et al. (1988) attempted to directly estimate
the magnitude of male-male competition in platyr- Competition levels also reversed the predicted di-
rhine primates. They ranked each species into a rection of dimorphism for the comparison between
competition level. The lowest level contained spe- single-male and multimale mating systems.
cies where males were not seen to compete much at Whereas Harvey et al. (1978) originally suggested
all. The highest level contained species in which that single-male groups should show the greatest
male-male competition occurred in the context of degree of dimorphism based on differential male
year-round agonistic dominance hierarchies. Kay et reproductive success, competition levels predicted
al. (1988) found a strong relationship between com- that multimale groups with agonistic dominance hi-
petition levels and canine dimorphism. erarchies should show the greatest degree of dimor-
Plavcan and van Schaik (1992) formalized the phism based on high-frequency, high-intensity com-
competition level system, and applied it to all an- petition.
thropoids. They used dichotomous estimates of the Competition level 1 species are all monogamous or
intensity and potential frequency of male-male com- polyandrous. Plavcan and van Schaik (1992, 1997b)
petition. Intensity was defined as whether males are noted that such species are not necessarily charac-
tolerant or intolerant of one another. Potential fre- terized by an absence of male-male competition. For
quency was basically a dichotomous demographic example, male hylobatids are known to be relatively
measure of whether one, or more than one, male intolerant of one another, but engage in low-fre-
typically occurred with a group of adult females. If quency competition. Technically, they should be
more than one adult male occurred in a group, ago- placed in competition level 3. However, because hy-
nistic competition could potentially happen on a lobatids form pair-bonds, and females help to defend
daily basis. The low-frequency class also contained territories (hence technically also showing high-in-
species in which males were normally tolerant, ex- tensity, low-frequency competition), dimorphism is
cept during a limited breeding season, as well as not expected to evolve in hylobatids as a conse-
species typified by single-male harems with multi- quence of male-male competition. In a separate
male influxes during a limited breeding season. In- analysis of relative male canine size (not canine
tensity and potential frequency classifications were dimorphism), Plavcan (1993a) demonstrated that
combined into four competition levels. Dimorphism hylobatid male canine size is consistent with other
in both canine tooth size (Plavcan and van Schaik, competition level 3 anthropoids.
38 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
Plavcan et al. (1995) noted that, like males, female tooth size dimorphism. Plavcan (1999) suggests that
primates compete agonistically. Consequently, if ag- competition levels, which are strongly associated
onistic competition generates selection to develop or with canine dimorphism, may measure the utility of
maintain big canine teeth in male primates, then it canine teeth both as weapons, and as display items.
should do so in females too, as long as there is a It may be that high-frequency competition (which
fitness consequence to winning and losing fights. may or may not be associated with a higher or lower
Plavcan et al. (1995) classified male and female an- OSR) favors the enhanced development of weaponry
thropoids separately by intensity and potential fre- for display. This follows from the idea that physical
quency, generalizing the definitions above to apply competition is potentially dangerous, even to the
to males and females. However, they also noted that winner of a fight. Hence, in the high-frequency,
many female anthropoid primates (and males of a high-intensity classification, selection may favor
few species) compete agonistically in the context of larger canines in order to reduce the actual fre-
coalitions. That is, the outcome of fights is not de- quency of physical contact, by allowing the resolu-
termined by individuals, but by groups of individu- tion of conflicts through display rather than fighting.
als that support each other. In this case, Plavcan et This idea is not new (e.g., Crook, 1972; Leutenegger
al. (1995) reasoned that weaponry should not play as and Kelly, 1977; Harvey et al., 1978), and the result
prominent a role in determining the outcome of is consistent with the observed modest correlation
fights, and hence that animals that regularly com- between canine dimorphism and body mass dimor-
pete in coalitions should have smaller canine teeth phism (Leutenegger and Kelly, 1977; Plavcan and
than those that compete in high-intensity, high-fre- van Schaik, 1997b).
quency dyadic contexts. Plavcan et al. (1995) found a Taken together, comparisons of competition lev-
significant effect of frequency, intensity, and coali- els, competition classifications, and the OSR present
tionary competition in both male and female anthro- a clearer picture of the relationships between sexual
poids. The analysis was the first to demonstrate a selection, social systems, and sexual dimorphism.
link between female agonistic behavior and female On the one hand, it seems that sexual selection is
canine size. Clearly, canine dimorphism is a func- indeed an important factor in the evolution of body
tion of selection on both male and female characters. size and canine tooth size dimorphism. On the other
Another important paper came in the application hand, sexual dimorphism is clearly a function of
of a concept known as the operational sex ratio variation in both male and female traits. For exam-
(OSR). The theory was laid out by Emlen and Orling ple, while canine tooth size in both sexes may vary
(1977), but not applied to primates until 1996 (Mi- as a function of male and female agonistic competi-
tani et al., 1996). Emlen and Orling (1977) noted tion, such competition may be over mates or re-
that differential male reproductive success should sources, and the weaponry may be selected for either
be a function not only of the sex ratio in a popula- its effectiveness in physical combat, or display in
tion, but also of the actual ability of males to mo- preventing combat. This strongly implies that the
nopolize access to females. In primates, this should evolution of dimorphism is not truly a function of
be a function of when females become receptive and differential male reproductive success; rather, it is a
fertile relative to one another. Hence, if female es- function of differential selection for the development
trus and ovulation do not overlap in timing, a single of male and female traits (Leigh, 1992, 1995a,b;
male can successfully guard each female in a group, Martin et al., 1994; Plavcan et al., 1995). In this
one at a time, preventing the other males from sense, sexual dimorphism can be thought of as re-
breeding. However, if females come into estrus and flecting the fact that male and female traits are
ovulate simultaneously, a male can only guard one influenced by different functional and selective re-
female at a time, meaning that other males will be gimes, which may vary substantially among species
able to successfully mate and reproduce. Mitani et that are classified as superficially sharing similar
al. (1996) applied this concept to a sample of 18 mating systems. This may seem obvious, but for
polygynous anthropoid primates, and found a signif- many years the evolution of sexual dimorphism in
icant association between the operational sex ratio primates was seen as a function of sexual selection
and body mass dimorphism. This strongly suggests acting on male traits, with the female serving as a
that previous analyses failed to corroborate the sex- baseline of comparison only.
ual selection hypothesis using mating systems, be-
cause mating systems do not capture variation in Sperm competition. One other form of male-male
sexual selection. The result also reinforces the im- competition has received a great deal of attention in
portance of focusing on differential male reproduc- recent years; sperm competition (Harcourt and
tive success associated with male-male competition Gardiner, 1994; Harcourt, 1995; Dixson, 1997). Ag-
in the evolution of sexual dimorphism. onistic male-male competition occurs before copula-
Interestingly, the OSR is not correlated with ca- tion. However, if a female is inseminated by several
nine tooth size dimorphism. The reasons for this are males, then the male producing the most sperm has
not clear. Plavcan (1999) suggests that it might be a the greatest chance of producing offspring. The
function of either small comparative sample sizes, or chances of fertilizing an egg might also increase if a
a different selective mechanism operating on canine male produces sperm that are faster or more capable
J.M. Plavcan] DIMORPHISM IN PRIMATES 39
1
TABLE 3. Mechanisms of mate choice that potentially may influence dimorphism in primates
Mechanism Effect
Females favor male trait that signals male fitness or Exaggerated male pelage, color, size
quality
Females incite male-male competition to mate with Larger male size, weaponry; exaggerated female
strongest, healthiest males displays favored by males
Females prefer males that can defend against Larger male size, weaponry
infanticidal males
Females confuse paternity by mating with multiple Reduced male size, weaponry through tempering
males to defend against infanticide of differential male reproductive success; female
displays that conceal ovulation, but attract
males
Female reduction of group size to reduce likelihood Reduced male size, weaponry through tempering
of takeover by infanticidal male of differential male reproductive success;
increased female weaponry reduces canine
dimorphism
1
See text for detailed discussion and references.
histochemically of fertilizing an egg. While these there is anecdotal evidence for the important role
latter mechanisms may play some role, there is over- that mate choice may play in the evolution of dimor-
whelming evidence that testicular volume, density phism.
of seminiferous tubules, and seminal vesicle size are Female mate choice can take several different
greater in species with multimale mating systems, forms among primates (Table 3). In the classic model
where females mate with more than one male (Har- of mate choice, females express a preference for
court and Gardiner, 1994; Harcourt, 1995; Dixson, males bearing a certain trait which presumably sig-
1997). Species such as Brachyteles and Pan are no- nals greater male quality. The trait can be morpho-
torious in that male-male agonistic competition is logical, as in the bright plumage of many birds, or it
not intense, mating is promiscuous, and testicular can be behavioral, as in the nest-building activities
volume is relatively enormous. In fact, testicular of the bower bird. For example, antler development
volume is relatively larger in most multimale spe- in white-tailed deer is correlated with male health
cies showing polyandrous mating. Conversely, mo- (Ditchkoff et al., 2001). Crook (1972) speculated that
nogamous species, and those characterized by sin- the large mane of male Theropithecus serves to en-
gle-male groups, show relatively small testicular hance the apparent body size dimorphism of this
volume. species, a tactic that may be favored in an environ-
Sperm competition illustrates that sexual selec- ment scarce in resources. However, body size dimor-
tion in primates is not simply a function of whether phism in Theropithecus is similar to that seen in
males fight for females or not. Males and females other papionines, suggesting that this might not be
both have reproductive strategies which often con- the case. Female Theropithecus play an active role in
flict, leading to the evolution of strategies and coun- selecting a mate (Stammbach, 1987), so it would not
terstrategies. Sperm competition reflects just such a seem unreasonable to speculate that females select
process. Absent the opportunity to overtly or com- male consorts on the basis of pelage condition, which
pletely exclude one another from access to females in in turn might reflect male health.
the first place, males pursue competition within the Females may also incite male-male competition in
female reproductive tract. order to choose the winner of a fight. For example,
Mate choice. The role of mate choice in the evo- Pagel (1994) speculated that female estrous swell-
lution of sexual dimorphism in primates has re- ings in catarrhines evolved as a result of female-
ceived less attention than mate competition. Recent female competition, inciting the most fit males to
years have seen an increase in the literature dis- invest heavily in competition for females with the
cussing female mating strategies (e.g., Small, 1989; most exaggerated swelling. Though this hypothesis
Smuts and Smuts, 1993; Nunn, 1999; van Schaik et receives little comparative support (Nunn, 1999;
al., 1999; Stallmann and Froehlich, 2000). These Stallmann and Froehlich, 2000), there is clear evi-
involve explicit female choice, as well as various dence that female macaques and baboons prefer to
female strategies to counter male mating coercion mate with dominant males (Kappeler, 1999; Nunn,
and domination (Smuts and Smuts, 1993). There 1999; van Schaik et al., 1999).
has been no quantitative comparative analysis of Recent years have seen growing evidence of the
how female choice and female mating strategies critical role that infanticide plays in shaping male/
might affect the expression of sexual dimorphism in female interactions. Smuts and Smuts (1993) point
any character, apart from estrous swellings in ca- out that males should attempt to monopolize access
tarrhines (Pagel, 1994; Nunn, 1999; Stallmann and to females in any way possible, including physical
Froehlich, 2000). This probably reflects the fact that coercion. The most extreme form of coercion is in-
mate choice is difficult to quantify. Nevertheless, fanticide, in which the male kills a females offspring
40 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
in order to bring about estrus. Given that females ters between females could possibly select for larger
are limited in the number of offspring they can pro- female canines, further reducing dimorphism.
duce, there should be powerful incentives for fe- Finally, females may seek dominant males for pro-
males to develop counterstrategies against infanti- tection from infanticidal males (Sterk, 1997; Kap-
cide. peler, 1999). In single-male species, infanticide fol-
Two ways of defending against infanticide should lows male takeover of a group. Hence, association
affect the evolution of dimorphism in primates: a with a dominant male may help protect female off-
female can either confuse paternity so that a male spring from infanticidal males, and may be a pri-
cannot be certain that he is killing his own offspring, mary factor in the formation of groups in some spe-
or a female can associate with a male who will pro- cies. It is tempting to speculate that extreme body
tect her from other infanticidal males. size dimorphism in gorillas reflects differential male
It is widely hypothesized that females in multi- reproductive success that is enhanced or driven by
male groups mate polyandrously in order to confuse strong female choice.
paternity (e.g., Small, 1989; Smuts and Smuts,
1993; Pagel, 1994; Nunn, 1999; van Schaik et al., Models for other causes of dimorphism
1999; Stallmann and Froehlich, 2000). Females in As noted above, the importance of factors other
single-male groups are known to seek out sneak than sexual selection on dimorphism has been long
matings with extragroup males. This is thought to debated. While recent studies have corroborated and
guard against infanticide in the event of a male elaborated the importance of sexual selection and
takeover (most infanticide in single-male groups oc- intrasexual competition in the evolution of dimor-
curs immediately after a male takeover). In multi- phism, they have also confirmed the complexity of
male groups, recently immigrated males are most forces that drive or constrain the evolution of dimor-
likely to commit infanticide. Consistent with this is phism. Dimorphism in various traits is known to be
that females actively seek out matings with recent correlated with body mass, diet, substrate, phylog-
immigrant males (van Schaik et al., 1999). eny, and even rainfall. Each of these correlations
Paternity confusion should affect the evolution of may reflect a variety of different mechanisms affect-
dimorphism by tempering the effect of male-male ing the expression and evolution of dimorphism.
competition on differential male reproductive suc-
cess, but the magnitude of such an effect may be Body size. Sexual dimorphism in body mass and
extremely difficult to measure. While multiple mat- canine tooth size is correlated with overall body size
ings might confuse paternity, they do not mean that (Clutton-Brock et al., 1977; Harvey et al., 1978; Leu-
male dominance has no benefit to males. For exam- tenegger and Cheverud, 1982, 1985; Gautier-Hion
ple, Nunn (1999) hypothesized that exaggerated es- and Gautier, 1985; Cheverud et al., 1985; Plavcan
trous swellings in female catarrhines serve as grad- and van Schaik, 1992, 1994, 1997b; Pickford, 1986;
ed signals of female fertility in multimale groups. Plavcan, 1999). This phenomenon has been docu-
In this model, females prefer to mate with the dom- mented across a wide variety of animals (Rensch,
inant male at the time most likely to result in fer- 1960), and remains a topic of much discussion (Re-
tilization, but also want to confuse paternity to iss, 1986; Andersson, 1994; Fairbairn, 1997). The
guard against infanticide. Dominant males guard model of Leutenegger and Cheverud (1982, 1985)
females at maximum tumescence only, allowing explained this as a function of greater male charac-
other males to mate with the female at other points ter variability, but, as previously reviewed, their
in her cycle. However, there is not an exact corre- analysis has been subject to much criticism.
spondence between ovulation and maximum tumes- Other mechanisms may explain the correlation.
cence. Hence, while the dominant male has the Clutton-Brock et al. (1977) suggested five mecha-
greatest chance of siring offspring, other males will nisms that might explain the relationship: 1) Selec-
also have a chance of siring offspring, thereby con- tion for larger male size might also favor larger
fusing paternity. If true, then female choice counters female size as a correlated response. 2) At large
male infanticide, and both dampens and maintains size there are fewer competing species, freeing
differential male reproductive success resulting males to increase size without facing ecological com-
from agonistic competition. petition. 3) It may be energetically cheaper to in-
A more recent hypothesis is that female primates crease male body size at larger sizes. 4) Selection
regulate group size in order to avoid infanticide may favor size differences to reduce feeding compe-
risks (Pope, 2000). In this model, the probability of tition at larger sizes, if larger species tend to feed on
male takeover of a group is proportional to group low-density food distributed in clumps. 5) There
size. Because infanticide usually follows a male might be greater pressure to reduce female body size
takeover, females may evict other females in order at larger sizes in order to speed female maturation
to keep group size down. If true, this might limit so that they can breed at a younger age. Kappeler
differential male reproductive success by limiting (1990, 1991) suggested that the lack of mass dimor-
the number of females that a male can monopolize, phism in strepsirrhines might be explained if, at
hence limiting selection for the development of smaller body size, selection favors speed and agility
weaponry. At the same time, such agonistic encoun- over increase in male body mass or canine tooth size.
J.M. Plavcan] DIMORPHISM IN PRIMATES 41
Other studies suggest that there may be a causal phic catarrhines, while folivorous howler monkeys
relationship between body size and sexual selection. are the most dimorphic platyrrhines. Correlations
At larger body sizes, females tend to form large between diet and either canine or body mass dimor-
groups, which makes it easier for males to try to phism are not significant in controlling for male-
exclude other males from access to females. Mitani male competition levels (Plavcan and van Schaik,
et al. (1996) noted that their estimate of the opera- 1992, 1994, 1997b). The idea that male-male compe-
tional sex ratio is significantly correlated with body tition might be less intense in folivorous species
mass, while Plavcan and van Schaik (1997b) noted through an energetic constraint (Leutenegger and
that competition levels are also correlated with body Kelly, 1977; Milton, 1985) is contradicted by the
size. Unfortunately, all of these models are contra- intense male-male competition seen in some foli-
dicted by the observation that small (1,000 g) early vores (e.g., Presbytis thomasi, Procolobus verus, Go-
anthropoids were sexually dimorphic in body size rilla gorilla; Plavcan and van Schaik, 1997b). Alter-
(Simons et al., 1999). This suggests that no current natively, females of folivorous species tend to be
model satisfactorily explains the link between size more dispersed in association with scramble com-
and dimorphism in living primates. petition, possibly limiting male differential repro-
The mechanism underlying the correlation be- ductive success (Plavcan and van Schaik, 1994), but
tween size and dimorphism has strong implications this idea is difficult to test, and again fails to explain
for the way that dimorphism should be measured in the strong dimorphism of some folivorous species.
comparative analyses. If dimorphism is a direct Thus, the weight of evidence suggests (albeit incon-
function of increasing body size, then it is appropri- clusively) that diet is not an important factor di-
ate to measure relative dimorphism as a residual rectly affecting the evolution of dimorphism.
from a regression of dimorphism against body size Careful scrutiny reveals that, controlling for esti-
(e.g., Ford, 1994; Mitani et al., 1996). Allometric mates of male-male competition, the only folivorous
adjustment of dimorphism assumes that there is a anthropoids that show usually weak body mass di-
nonadaptive baseline of dimorphism contingent on morphism are colobines. Interestingly, many folivo-
size, with sexual selection modifying the expression rous colobines also show strong canine dimorphism
of dimorphism. However, if dimorphism covaries (Plavcan and van Schaik, 1997b). The strong canine
with body size through an interaction between body dimorphism and intense male-male competition
size and female grouping pattern, sexual selection, suggest that sexual selection operates in these ani-
and male mating competition, then regression of mals as in other anthropoids. This in turn suggests
dimorphism against size will remove the correlation that the lack of mass dimorphism could reflect a
between sexual selection and dimorphism, inappro- situation where body mass either is no longer im-
priately biasing against corroboration of the sexual portant in determining the outcome of fights, or is a
selection hypothesis. Unfortunately, allometric re- constraint on the evolution of body mass dimor-
gression of dimorphism is too often taken as a given, phism. It is interesting to note that large folivorous
with little attention given to the underlying assump- species (gorillas and proboscis monkeys) tend to
tions. Recent comparative analyses (Kappeler, 1990, show intense body mass dimorphism, whereas
1991; Godfrey et al., 1993; Mitani et al., 1996; Plav- smaller folivorous species do not. Perhaps there is a
can and van Schaik, 1997b; Plavcan, 1999) suggest balance between pressure to limit body mass in as-
that the adage that correlation does not equal cau- sociation with locomotion (see below), and to in-
sation needs to be heeded in this case, and allomet- crease it in order to slow gut-passage time in order
ric adjustment of dimorphism should be avoided to make digestion more efficient. Hence, low body
without careful justification. Rather, attention mass dimorphism may reflect pressure to maximize
should be directed first to testing hypotheses about female body mass in smaller folivorous species. Con-
the causal relationships between dimorphism, size, versely, the dissociation might reflect an interaction
behavior, and ecology. between feeding, locomotion, and substrate use.
Colobine primates tend to be leapers exploiting
Diet. Several studies have suggested that body leaves and fruits on small branches, and they tend to
mass dimorphism is linked to diet. Leutenegger and be large. Hence, there may be a constraint on colo-
Kelly (1977) and Milton (1985) suggested that a bine male body size that limits the expression of
low-energy, folivorous diet may constrain either the body mass dimorphism (Leutenegger and Kelly,
expression of dimorphism, or male-male competi- 1977).
tion. Conversely, Ford (1994) and Mitani et al. Greenfield (1992a, 1998) suggested that canine
(1996) suggested that a folivorous diet might allow tooth size reduction, and hence reduction in canine
males to become larger, leading to enhanced mass tooth size dimorphism, reflects pressure to incorpo-
dimorphism. rate the canine teeth into an incisal functional field.
Diet is only weakly associated with variation in Greenfield (1992a, 1998) noted that the develop-
dimorphism in that folivorous species tend to be less ment of the mesial cristid on the mandibular canine,
dimorphic than other species. However, this rela- which occludes with the lateral maxillary incisor in
tionship is very loose: proboscis monkeys and goril- many anthropoids, is inversely correlated with man-
las are folivorous, and are among the most dimor- dibular canine crown height. He suggested that de-
42 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
velopment of this contact is the primary driving Kelly, 1977). Female group size may be larger in
force behind canine reduction in anthropoid pri- more terrestrial species, leading to greater male-
mates. Plavcan and Kelley (1996) noted that while male competition. Alternatively, females may be
the mesial cristid may reflect a functional contact, easier to guard in a two-dimensional, open habitat
the hypothesis does not necessarily explain maxil- than in a three-dimensional closed habitat. Such
lary canine reduction: strepsirrhine primates com- hypotheses are difficult to prove, but the consistency
pletely incorporate the mandibular canine into a of the observation strongly suggests that some
functional incisal field (in this case, the tooth comb), mechanism associated with substrate use constrains
without concomitant reduction of the maxillary ca- or enhances dimorphism.
nine. In fact, they redevelop the mandibular P2 to
function as a canine. This demonstrates that func- Correlated response. Correlated response is an-
tional alterations (be they dietary or otherwise) of other factor that can influence the expression of
the mandibular canine need not dictate any reduc- dimorphism. Correlated response is the phenome-
tion of the maxillary canine. non whereby a character that is functional in one
There is one clear case of a dietary effect on canine sex appears in the other because the genes for the
dimorphism. Pithecine primates use their canine trait are not located on the sex chromosomes (Lande,
teeth to open hard fruit (Kinzey, 1992). The canines 1980). In other words, if the genes determining a
of both sexes are enlarged and modified to look like trait are not located on the sex chromosomes, then
chisels. Canine dimorphism in pithecines species is selection that favors a change in the trait in one sex
modest or absent, undoubtedly reflecting this di- should automatically produce the same change in
etary specialization (Greenfield, 1992a,b, 1998; both sexes. Lande (1980) showed that if selection
Plavcan and Kelly, 1996). favors the trait in one sex, but that the trait is
In summary, there is only very weak evidence for disadvantageous in the other sex, then selection
a causal relationship between dimorphism and diet should favor some mechanism to decouple the ex-
in primates. No mechanism (energetic constraints, pression of the trait between sexes. However, the
metabolic constraints, association between diet and time necessary for this could be quite long.
female dispersal patterns, locomotor constraints, or The phenomenon is particularly interesting be-
selection to turn canines into incisors) adequately cause the model predicts that dimorphism will
explains the very weak correlation between diet and evolve by the reduction of a trait in one sex. For
dimorphism seen across all anthropoids. While this example, selection may have initially favored the
does not rule out an important role for diet in the development of large male canines in the ancestral
evolution of dimorphism, it suggests that any such anthropoid, producing large canines in both sexes.
role is secondary to the effects of sexual selection. Canine dimorphism would then have evolved if large
On the other hand, dietary specialization of the ca- canines are somehow disadvantageous in females,
nine teeth clearly affects canine dimorphism in some producing selection favoring a decoupling of genetic
species. control of male and female tooth size, and reduction
Terrestriality. It is well-known that terrestrial in female canine size.
species tend to be more dimorphic than arboreal Greenfield (1992a, 1998) attributes variation in
species (Crook, 1972; Clutton-Brock et al., 1977; anthropoid female canine size primarily to corre-
Harvey et al., 1978; Leutenegger and Kelly, 1977; lated response. Female relative canine size is corre-
Gaulin and Sailer, 1984; Cheverud et al., 1985; Gau- lated with male relative canine size across all an-
tier-Hion and Gautier, 1985; Plavcan and van thropoids (Greenfield, 1992a, 1998; Plavcan et al.,
Schaik, 1992, 1994, 1997b; Martin et al., 1994). This 1995; Plavcan, 1998). Plavcan (1998) demonstrated
is commonly thought to reflect greater predation that this relationship only holds across species in
pressure on terrestrial species, assuming that they which females show little or no agonistic competi-
are more susceptible to predators than arboreal spe- tion. In those species showing female agonistic com-
cies. If male primates are more susceptible to pre- petition, there is no correlation between relative
dation, either because they spend greater periods of male and female canine size. This suggests that
time alone, or because they more frequently defend correlated response affects female canine size, but
groups against predators, then larger size and does not constrain the evolution of large female ca-
larger canine teeth should be favored. Plavcan and nine size in association with agonistic competition.
van Schaik (1992) noted that savanna-dwelling spe- Greenfield (1996) presented evidence that corre-
cies are more dimorphic than forest-dwelling species lated response may affect the development of the
of the same competition levels, supporting this hy- honing premolars in female anthropoid primates,
pothesis. However, there are other reasonable expla- which appear to be larger than necessary to accom-
nations. For example, there is the hypothesis that modate the maxillary canine in many anthropoid
arboreal species face an upper body size limit: larger species. Correlated response may influence other an-
body size should constrain arboreal species from atomical characters in primates, but unfortunately
moving about the trees, especially on smaller sub- the mechanism has received little attention beyond
strates (Clutton-Brock et al., 1977; Leutenegger and that just mentioned.
J.M. Plavcan] DIMORPHISM IN PRIMATES 43
Niche divergence. There has long been specula- other words, they suggested that a species shows a
tion that niche divergence favors the evolution of particular degree of dimorphism because its ances-
size dimorphism in primates (Clutton-Brock et al., tor was dimorphic.
1977). The concept is derived from studies of birds, Phylogenetic constraint is sometimes used to ex-
which have shown that males and females some- plain phylogenetic correlations of characters. But
times differ in both size and diet, apparently to the term is ill-defined, and seems unsatisfactory as
reduce feeding competition between the sexes. There an explanation unto itself because it does not neces-
have been some indications that male and female sarily specify any particular mechanism, apart from
diets differ in orangutans and some other species. the fact that there is a correlation between a trait
However, dietary differences tend to be relatively and phylogeny. However, as far as dimorphism goes,
slight, and the niche divergence hypothesis has operational sex ratios, mating systems, modes of
never received much support. At least part of the locomotion, substrate preference, diet, and habitat
problem is that it is very difficult to tease apart the preference are also correlated with phylogeny (Clut-
causes of dietary differences between males and fe- ton-Brock et al., 1977; Harvey et al., 1978; Mitani et
males, and it is almost impossible to determine if al., 1996; Plavcan and van Schaik, 1997b; Plavcan,
any dietary differences drive the evolution of dimor- 1999). This raises the question of what, exactly,
phism, or whether dimorphism itself produces di- underlies such phylogenetic correlations? Do they
etary differences. reflect genetic constraints on the expression of char-
More intriguing is the suggestion that body mass acters, historical baggage from an ancestral condi-
dimorphism in part reflects selection for reduced tion, or canalized evolution reflecting a compromise
female body mass in association with dietary con- in the expression of multiple characters? These
straints (Demment, 1983; Martin et al., 1994). Fe- questions are extremely difficult to tease apart.
male primates spend a significant portion of their It has been suggested that dimorphism in Simias
adult lives pregnant or lactating, both of which rep- concolor and Cercopithecus neglectus are examples
resent significant metabolic commitments by fe- of phylogenetic inertia, on the basis that both spe-
males. It has been suggested that, metabolically, cies are monogamous (Leutenegger and Lubach,
female body size really should be measured as the 1987). In these cases, dimorphism is hypothesized to
sum of the females body mass along with that of her reflect a condition held over from an ancestor that
fetal or suckling offspring (Demment, 1983; Smith was probably polygynous. One can imagine a num-
and Jungers, 1997). If true, then body mass dimor- ber of hypotheses to explain the phenomenon: either
phism of many species might partly reflect a reduc- selection has not had time to reduce dimorphism (an
tion in female body mass in order to compensate for evolutionary time lag), selection cannot alter the
the demands of pregnancy and lactation. Of course, magnitude of dimorphism (because of some develop-
if this hypothesis were universally true, then we mental or genetic constraint on changes in male or
would have trouble explaining monomorphism. One female body size relative to each other), or perhaps
test might be to compare seasonality or resource there is no selective pressure to alter the degree of
availability during the pregnancy and lactation of dimorphism. However, while observations of male-
species showing similar mating systems, predicting female pairs are not doubted, Watanabe (1981)
that size dimorphism should be greater in environ- showed convincingly that S. concolor is monoga-
ments with less abundant resources. Of course, the mous only in areas subject to hunting pressure.
difficulty in doing this is accurately estimating the Other reports also suggest that C. neglectus is not
strength of sexual selection. monogamous throughout its range (Brennan, 1985).
This suggests that these two species might not be
Taxonomy. Dimorphism is strongly correlated clear cases of phylogenetic constraint.
with phylogeny (Cheverud et al., 1985; Leutenegger One of the most puzzling taxonomic patterns of
and Lubach, 1987; Martin et al., 1994; Plavcan and dimorphism is that between prosimians and anthro-
van Schaik, 1994, 1997b). I have already touched on poids. Strepsirrhines and tarsiers exhibit little or no
the pattern of weak mass dimorphism and strong sexual dimorphism in body mass, tooth size, or pel-
canine dimorphism in colobines, but other taxo- age, while anthropoids commonly exhibit extreme
nomic groups exhibit characteristic patterns of di- levels of dimorphism in one or more of these char-
morphism (Table 1). For example, papionines are all acters. Yet both groups are characterized by polyg-
strongly dimorphic, and most have exaggerated fe- yny and intense male-male competition in many
male estrous swellings. Callitrichine primates all species. Kappeler (1991) suggested that strepsir-
exhibit low levels of dimorphism coupled with either rhines exhibit little dimorphism because selection
monogamous or polyandrous mating systems. All favors fighting skills and agility rather than weap-
hylobatids are monogamous and show low levels of onry. Plavcan et al. (1995) noted that male and
dimorphism. The list can go on for different combi- female strepsirrhines tend to exhibit similar types of
nations of characters at different taxonomic levels. intrasexual competition, and suggested that the lack
Cheverud et al. (1985) demonstrated that a large of dimorphism reflects similar selection pressures
part of the variation in anthropoid body mass dimor- for the development of weaponry and size in males
phism is explained (statistically) by phylogeny. In and females. Plavcan (1998) suggested that corre-
44 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
lated response may explain the lack of canine dimor- of intrasexual competition. Unfortunately, there is
phism in strepsirrhines, though he noted that the not enough comparative evidence to make any judg-
equal male/female competition hypothesis of Plav- ment about female agonistic competition. Female
can et al. (1995) was still a viable explanation. Leigh guerezas do eat seeds, but so do other colobines.
and Terranova (1998) suggested that body mass di- Likewise, other anthropoid primates live in dry hab-
morphism is constrained in Malagasy lemurs as a itats, with females susceptible to predation, and
consequence of extreme seasonality in resource-poor there is little actual documentation of predation or
environments. All of these hypotheses are reason- predator defense among guereza subspecies. Re-
able, supported by data, and difficult to disprove. gardless of the cause, the variation in canine dimor-
In summary, it is now well-established that there phism among guereza subspecies is real and signif-
are strong phylogenetic correlations in dimorphism icant.
as well as the behavioral/ecological variables that ONTOGENY
are hypothesized to be causally linked to the evolu-
tion of dimorphism. The reasons for phylogenetic Most studies of sexual dimorphism focus on adult
correlations in all these variables are likely to vary. characters. However, sexual dimorphism in adults is
The evolution of phylogenetic patterns is itself in necessarily a product of different male and female
need of study. But regardless of the reasons under- growth trajectories. Shea (1986) pointed out that
lying the existence of these patterns, the strength of males can get larger than females either by extend-
phylogenetic correlations mandates that compara- ing a common growth trajectory and maturing later
tive analyses testing for general causal mechanisms than females (time hypermorphosis or bimatur-
of dimorphism across taxonomic groups must care- ism), or by growing faster than females in a given
fully control for phylogenetic correlations in the period of time (rate hypermorphosis). Likewise,
data, using modern comparative methods (e.g., dimorphism can be produced if females mature ear-
Cheverud et al., 1985; Pagel, 1994; Plavcan and van lier than males, or grow more slowly.
Schaik, 1994; Plavcan et al., 1995; Mitani et al., Leigh (1992) documented and quantified patterns
1996; Nunn, 1999). of growth in males and females of 38 primates, dem-
onstrating convincingly that size dimorphism arises
Epiphenomenal variation. An often unappreci- through variation in both time and rate hypermor-
ated factor contributing to sexual dimorphism is phosis. Most species showed some combination of
epiphenomenal variation. This is variation that re- both bimaturism and sex differences in growth rate.
sults from different environmental conditions which Most interesting was the fact that congeneric spe-
might affect growth and development, or even from cies could vary in the pattern of development lead-
local adaptation in subspecies of a widely spread ing to a particular degree of sexual dimorphism.
species. Populations and subspecies can differ in While adults of two closely related species might
dimorphism from one to another. Turner et al. show the same magnitude of body mass dimorphism,
(1994, 1997) demonstrated that Cercopithecus ae- one might achieve it through extended male growth,
thiops populations from different parts of Kenya while the other might achieve it through rate hyper-
differed significantly in body mass dimorphism, morphosis. Clearly, the magnitude of adult mass
largely as a result of changes in female body mass. dimorphism in a species is not constrained by the
Females from areas showing higher average rainfall ontogenetic pattern of dimorphism, but this raises
showed greater body mass than those from drier the question of why species should differ in the pat-
areas. More recently, Jones et al. (2000) presented tern of male and female development.
evidence that Alouatta palliata subspecies differ in Leigh (1995b) suggested that males can follow
the magnitude and pattern of sexual dimorphism, alternate developmental pathways as a response to
though the cause of this variation is unclear. selection pressure faced by juveniles. He found that
On a larger scale, Hayes et al. (1995) demon- most species in which adult dimorphism is achieved
strated variation in dimorphism and relative female through rate hypermorphosis live in single-male
canine tooth size in Colobus guereza. Guereza mon- groups, while those that achieve adult dimorphism
keys are peculiar in that females can possess enor- through time hypermorphosis tend to live in multi-
mous canine teeth. Variation in relative female ca- male groups. Leigh (1995b) suggested that this ob-
nine size among guereza populations is very high. servation is consistent with two models: juvenile
Clearly, canine tooth size sexual dimorphism in this risk aversion (Janson and van Schaik, 1993), and
species varies as a function of variation in female social complexity.
canine size. The reason for this variation has been a Janson and van Schaik (1993) pointed out that
continuing mystery. Hayes et al. (1995) noted that primates can be roughly divided into those that pur-
females from drier environments had significantly sue a fast life-history, in which development is
larger canines than those from wetter habitats. accelerated, and those that pursue a slow life-his-
They suggested that predation pressure favors large tory, in which development is prolonged. The juve-
female canines. Seed predation may be another ex- nile risk aversion model posits that rapid rates of
planation (with females using their canines to open growth are associated with higher mortality in pri-
hard fruit, as in pithecine primates), or higher levels mates, probably as a result of competition with
J.M. Plavcan] DIMORPHISM IN PRIMATES 45
adults. For male primates growing up in multimale troglodytes females. Likewise, gorilla females ma-
groups, a slow rate of growth will minimize compe- ture early, enhancing the magnitude of dimorphism.
tition with adults, both for food resources, and by This strongly implies that changes in the female
extending the period during which adult males do pattern of growth constitute an important compo-
not view juveniles as competitors for mates. Con- nent in the final magnitude of dimorphism.
versely, males from single-male groups are usually Leigh and Shea (1995) suggested that female
evicted from a group relatively early. This subjects growth trajectories are strongly linked to diet. Again
the male to greater risks, favoring rapid attainment referring to the model by Janson and van Schaik
of large body size. (1993) of juvenile risk aversion, they suggested that
The social complexity model posits a basic differ- female growth patterns are strongly influenced by
ence in social complexity between single-male and female competition over resources. Janson and van
multimale groups (Leigh, 1995b). The model as- Schaik (1993) suggested that species engaging in
sumes that in order to reproduce successfully, males contest competition over resources (largely associ-
growing up in multimale groups need longer periods ated with frugivorous diets, wherein resources are
of time to learn the social skills necessary to interact patchily distributed) will face greater juvenile risks
with and form social bonds with both adult males at faster growth rates, as a result of competition
and females. Such males normally experience a with adults over limited resources. In contrast, spe-
short period alone when they transfer from their cies characterized by scramble competition (largely
natal troop to a new troop. Before and after transfer, associated with folivorous diets) will not face in-
the male experiences an extended period of time in creased juvenile risks at high growth rates, because
which it is low in the resident dominance hierarchy. of an abundance of scattered resources. Leigh and
Essentially, these males can afford a period of time Shea (1995) suggested that in this latter case, selec-
during which they can increase in size, gain experi- tion can favor rapid female maturation and an ear-
ence, develop social skills, form alliances, and even- lier start to reproduction without increasing female
tually move up the dominance hierarchy to achieve juvenile mortality. Hence, gorillas and Pan panis-
reproductive success. In contrast, males living in cus, which are characterized by scramble competi-
single-male groups are evicted from their natal tion, show early female maturation (and smaller
troop when they become juveniles, and spend an body size), while P. troglodytes, which is character-
extended period of time either alone, or with a band ized by female contest competition, prolongs female
of other young males. Males may take over a troop of maturation in order to minimize juvenile risks. Im-
females, during which time they can monopolize portantly, Leigh and Shea (1995) also note the major
access to a group of females. Once evicted from their contribution of sexual selection through male-male
natal troop, their chances of successfully taking over competition to adult dimorphism. Thus, the final
another troop are low. Hence, long-term bonds with magnitude of adult dimorphism is a sum of selection
other individuals and social skills are not as impor- on males and females.
tant to these animals in gaining access to females. On the basis of indirect evidence, Martin et al.
Of course, both of these descriptions oversimplify (1994) suggested that body mass dimorphism among
the variety of social relationships seen among pri- anthropoid primates is primarily a consequence of
mates, but the generalization seems to have some reduced female body mass through early matura-
power. However, Leigh (1995b) notes that limited tion. They noted that brain size and molar tooth size
comparisons find no real difference in age of male are determined early in development, and tend not
maturity between multimale and single-male spe- to be dimorphic. They then predicted that if dimor-
cies, even though there are substantial instanta- phism is a function of extended male growth, then
neous differences in growth rates during ontogeny. males of dimorphic species should have relatively
Leigh (1995b) suggests that detailed evaluations of small brains and teeth by comparison to monomor-
growth rate differences during ontogeny are neces- phic species. They presented evidence that in fact
sary to completely evaluate both models. females of dimorphic species have relatively large
Leigh and Shea (1995) provided a detailed com- brains and teeth, suggesting a reduction in female
parison of growth, body mass dimorphism, and be- body size. Their conclusion was partly based on the
havioral ecology in living hominoids. They suggested observation of a failure to find a relationship be-
that orangutan males show an indeterminate in- tween body size dimorphism and male-male compe-
crease in body mass (they could demonstrate no tition. Since that time, however, Ford (1994), Mitani
point at which males ceased increasing in body et al. (1996), and Plavcan and van Schaik (1997b)
mass), and gorillas and Pan paniscus achieve size demonstrated such a relationship. Nevertheless,
dimorphism largely through bimaturism, while P. there is no reason that the observation might not be
troglodytes achieves it through an increase in the valid, and the hypothesis needs to be explored in
rate of male growth. More importantly, they noted greater detail.
that both species of Pan show similar levels of adult The results of these studies both complement and
dimorphism, but they achieve it through different contrast with those of Plavcan et al. (1995) on rela-
patterns of male and female development. Pan pa- tive male and female canine size. All studies clearly
niscus females show early maturation relative to P. demonstrate that dimorphism is a function of
46 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
changes in male and female characters. Leigh and ent types of juvenile risks, or as a function of male
Shea (1995) and Plavcan et al. (1995) both associate social strategies. Females may alter growth patterns
female contest competition with changes in dimor- as a function of dietary pressures, and/or as a func-
phism. However, Plavcan and van Schaik (1995) tion of pressure for altering reproductive rates.
associate noncoalitionary female contest competi-
tion with decreased canine dimorphism through se- DIMORPHISM IN THE FOSSIL RECORD
lection for enhanced female weaponry. In contrast,
Dimorphism in the primate fossil record
Leigh and Shea (1995) associate this type of compe-
tition with reduced dimorphism through prolonged Knowledge about dimorphism in the fossil record
female growth associated with reduction of female can be valuable for both species recognition and
mortality. Hence, the effects of contest competition reconstruction of social behavior. In the first place,
on canine and body size dimorphism are parallel, sexual dimorphism can be a source of variation in a
but the underlying mechanisms are very different. morphological sample. Where the sex of individual
Leigh and Shea (1995) and Leigh and Terranova specimens cannot be reliably determined, sexual di-
(1998) both suggested that the absence of body mass morphism can mimic interspecific variation (Gin-
dimorphism in living strepsirrhine primates reflects gerich and Schoeninger, 1979; Cope, 1993; Plavcan,
a constraint on growth trajectories due to extreme 1993b; Plavcan and Cope, 2001). This has been a
seasonality. Leigh and Terranova (1998) pointed out particular problem for those interested in human
that polygynous malagasy lemurs experience very evolution, where the question of two sexes or two
rapid rates of growth. At the same time, these ani- species has been a focus of controversy (e.g., Zihl-
mals live in highly seasonal environments and are man, 1985; Cole and Smith, 1987; Leutenegger and
forced to resort to low-quality resources during part Shell, 1987; Kimbel and White, 1988; Miller, 1991,
of the year. This places a premium on rapid body- 2000; Wood, 1993; Kramer et al., 1995; Richmond
size increase. The highly restricted breeding season and Jungers, 1995; Lockwood et al., 1996; Lockwood,
may also select strongly for a limit on the timing of 1999). In the second place, the association between
male maturation. Hence, the combination of pres- sexual dimorphism and male-male competition and
sure for rapid growth and early maturation may mating systems means that it has often served as
limit the ability of males to achieve larger size than the only direct evidence for social behavior in the
females by constraining bimaturism, and capping fossil record (e.g., Wolpoff, 1976; Fleagle et al., 1980;
growth rates in both males and females. Gingerich, 1981, 1995; Lovejoy, 1981; Leutenegger
Finally, work has recently begun comparing and Shell, 1987; Foley and Lee, 1989; Kelley, 1989;
growth rates of canine teeth between male and fe- Krishtalka et al., 1991; McHenry, 1994a,b; Plavcan
male primates. Schwartz and Dean (2001) demon- and van Schaik, 1997a; Simons et al., 1999; Plavcan,
strated that canine dimorphism in living hominoids 2000a).
is a function of time hypermorphosis. Male canines Apart from this, a survey of what is known about
tend to grow for longer periods of time than those of sexual dimorphism in the fossil record reinforces
females, but not at a different rate. Though their and expands our knowledge of the causes and ex-
comparative sample was small, the results are in- pression of dimorphism in primates. Evidence from
triguing. It will be interesting to compare rates of the fossil record demonstrates that dimorphism (and
female canine development between species show- therefore probably polygyny): 1) arose early in an-
ing different relative female canine sizes. thropoid evolution and at small body sizes (Simons
In sum, there is a growing literature on the ontog- et al., 1999); 2) has arisen independently in different
eny of dimorphism which promises to shed consid- primate lineages (Krishtalka et al., 1991); and 3) in
erable light on the different mechanisms by which a number of species probably substantially exceeded
animals achieve dimorphism. These studies have that observed in the most dimorphic living primates
demonstrated that the magnitude of adult dimor- (Kelley and Xu, 1991; Kelley and Plavcan, 1998).
phism reflects any one of a combination of extended Catopithecus and Proteopithecus provide the ear-
male growth, shortened female growth, more rapid liest evidence of sexual dimorphism in the anthro-
male growth, or slower female growth. It is interest- poid fossil record so far (Simons et al., 1999). Both of
ing to note that the magnitude of adult dimorphism these early anthropoids were small (substantially
is not contingent on any particular growth path: two less than 1,000 g), demonstrating that the evolution
species can share the same level of dimorphism in of sexual dimorphism itself is not a function of the
adults that is achieved through different combina- evolution of large body size. This is reinforced by the
tions of male and female growth trajectories. This observation that Apidium, another small, slightly
suggests that sexual selection favoring adult dimor- younger early anthropoid, was strongly dimorphic
phism works in concert with, and not against, dif- (Fleagle et al., 1980). The presence of sexual dimor-
ferent selective pressures on juvenile growth trajec- phism in these species implies polygyny, suggesting
tories. There is growing evidence that different that high operational sex ratios and male-male com-
ontogenetic pathways reflect different selective petition are not a function of the evolution of large
pressures on males and females. Males might alter size (Simons et al., 1999), and that the correlation
developmental pathways in association with differ- between body mass and sexual dimorphism in living
J.M. Plavcan] DIMORPHISM IN PRIMATES 47
primates reflects the absence of strongly polygy- sexual dimorphism in early adapids has been used
nous, small-bodied, living anthropoids. Why such as evidence for an adapid origin for anthropoids
species are absent today is an interesting question, (Covert and Williams, 1994). Given that dimorphism
but small size alone is not the reason. has arisen independently in carnivores, ungulates,
The correlated response model discussed above pinnipeds, macropods, primates, cetaceans, and nu-
makes a clear prediction about the evolution of di- merous other vertebrate and invertebrate groups, it
morphism in early primates. If this model is true, would not be surprising that the character has
then it implies two things about dimorphism in early arisen independently in different primate lineages.
anthropoids. First, the earliest anthropoids, or their The variability in the magnitude of the character
immediate ancestors, may have been characterized among extant anthropoids would suggest that the
by large canine teeth in both sexes, if the primitive simple presence of dimorphism alone constitutes
condition for preanthropoid primates was small ca- only weak evidence for a link between anthropoids
nines in both sexes, coupled with solitary habits. and adapids.
Paleocene mammals such as Purgatorius came Sexual dimorphism has been documented in most
equipped with small canine teeth in both sexes, sup- later anthropoid taxa, including oligopithecids,
porting the hypothesis that canines were small in parapithecids, early catarrhines, most hominoids,
the ancestral primates, while other evidence sug- and early hominids (Ross et al., 1998, provide a
gests nocturnality and therefore probably solitary tabular summary). Miocene apes offer one of the
habits in the ancestral primate (Ross et al., 1998). If most intriguing pictures of sexual dimorphism, first
true, an increase in canine size in both sexes, and because they demonstrate unique aspects of dimor-
not the appearance of canine dimorphism, should phism not seen in living species, and second because
have accompanied the evolution of polygyny in the the ancestral hominid condition presumably arose
earliest anthropoids. This implies, in turn, that the from a Miocene ape pattern. Dimorphism appears to
evolution of dimorphism would have lagged behind be common among Miocene apes, most of which dis-
the evolution of polygynous mating systems. In this play large, easily recognizable male canine teeth
model, monomorphism resulting from big canines in and substantial size dimorphism (Kelley, 1986,
both sexes would not be indicative of monogamy or 1993, 1995a; Kelley and Xu, 1991).
polyandry. Highly intriguing is the likelihood that a number
The second implication is that the evolution of of Miocene hominoids were more dimorphic than
canine dimorphism in primates may have arisen any living primate. The most extreme example is
through a reduction in female canine size. If so, then Lufengpithecus. The hominoid dental samples from
the emergence of canine dimorphism in early an- Lufeng, China, are highly variable. It has been sug-
thropoids should track the dissociation of genetic gested that this reflects the presence of two species
control over male and female canine size, and should at the site (Wu and Oxnard, 1983a,b; Martin, 1991;
indicate not an increase in male-male competition, Cope and Lacy, 1992, 1994; Plavcan, 1993b). How-
but a decrease in female-female competition. All this ever, others maintain that the sample is composed of
is speculative. However, given the rapid increase in a single, extremely dimorphic species (Wu, 1987;
the number of Eocene primates being discovered in Kelley and Etler, 1989; Kelley and Xu, 1991; Wood
Asia and Africa, it provides an interesting basis for and Xu, 1991; Kelley, 1993). Most recently, Kelley
interpreting the meaning of the evolution of canine and Plavcan (1998) demonstrated that the pattern of
teeth in these animals. metric variation in the sample is most consistent
There is evidence of dimorphism in Eocene adapid with the presence of a single species more dimorphic
primates. Cantius and Notharctus both were char- than any living hominoid. The extreme dimorphism
acterized by sexually dimorphic canine teeth, and of Lufengpithecus opens up the possibility that apes
possibly substantial body mass dimorphism (Gin- from other Miocene localities were also so character-
gerich, 1981, 1995; Krishtalka et al., 1991). There ized. This leads to the question of what drove such
has long been an argument over whether living an- extreme dimorphism. Was it extreme sexual selec-
thropoids arose from or are the sister taxon of either tion? Perhaps there was selection to reduce female
Eocene adapids or omomyids. Current models for body size. Perhaps there was some relaxation of
anthropoid origins suggest that living tarsiers are constraints on male body size, allowing runaway
the extant sister taxon of anthropoids, to the exclu- evolution of large male size. Perhaps males differed
sion of strepsirrhines, and that omomyids are the ecologically from females. Unfortunately there is no
sister taxon of anthropoids from the Eocene, to the way to eliminate most hypotheses with current in-
exclusion of adapids (Ross et al., 1998). If adapids formation. Nevertheless, the topic is highly interest-
did not give rise to anthropoids, then sexual dimor- ing and deserving of much greater attention, be-
phism has clearly evolved more than once within cause an understanding of this phenomenon is likely
primates. Furthermore, if adapids are ancestral to, to provide a wealth of information about the life-
or the sister taxon of, living strepsirrhines, then the history and behavior of these animals.
lack of dimorphism in this extant group may not Not all Miocene apes were characterized by ex-
reflect a direct genetic constraint on the expression treme dimorphism. Dendropithecus, though dimor-
of dimorphism. On the other hand, the presence of phic, was characterized by large canine teeth in both
48 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
males and females, suggesting a hylobatid-like mat- is not a feature that unites all hominids. However,
ing system, or at least high-intensity intrasexual these figures need to be approached with great cau-
competition in both males and females (Fleagle, tion. First, sample sizes are small, meaning that
1999). Afropithecus canine dimorphism appears to dimorphism could easily be overestimated, espe-
be reduced through specialization of male and fe- cially by simply estimating dimorphism as a ratio of
male canines for opening hard fruit, analogous to the largest to smallest specimens available. Second,
modern pithecines (Leakey and Walker, 1997). Re- among primates, dimorphism of the occlusal dimen-
cently, Alba et al. (2001) suggested that canine re- sions of canine teeth (as opposed to the crown height
duction in Oreopithecus indicates the evolution of of the tooth) is poorly correlated with behavioral
chimpanzee-like mating systems, or at least sug- estimates of male-male competition. Plavcan and
gests a reduction in levels of male-male competition. van Schaik (1997a) argue that dimorphism of occlu-
They also suggested that the pattern of canine and sal dimensions is unreliable, except in extreme
dental reduction in Oreopithecus indicates overall cases, for inferring anything about social behavior in
neoteny throughout the dentition of these animals. primates. Nevertheless, A. anamensis is tantalizing
Bonis and Koufos (2001) suggested that canine re- in that it opens up the possibility of greater variabil-
duction in Ouranopithecus is a shared derived fea- ity in canine size and dimorphism among early
ture with hominids. However, Kelley (2001) demon- hominids than has previously been suspected.
strated that male canines in Ouranopithecus are as Ardipithecus ramidus has been claimed to lie at
substantial as in any other Miocene ape. the base of the hominid radiation (White et al.,
Dimorphism in hominids 1994). If the common ancestor of chimpanzees and
humans predates Ardipithecus by a relatively short
One of the key defining characters of hominids is time, this suggests either that canine reduction hap-
canine reduction (White et al., 1994; Fleagle, 1999). pened rapidly in the earliest hominids, or that large
Australopithecus afarensis, A. africanus, Paranthro- canine size reevolved in chimpanzees. The former
pus robustus, and P. boisei show small canines by hypothesis seems the more likely, though of course
comparison to living hominoids (Plavcan and van only more data from the fossil record can give us a
Schaik, 1997a) and modest to slight canine dimor- reliable picture of the evolution of canine dimor-
phism. This statement needs to be qualified. In dis- phism at this time.
cussing canine tooth size in hominids, it is common In contrast to the canine teeth, dimorphism in
to refer to the canines as large, big, or robust by hominid body mass was apparently quite substan-
comparison to those of Homo. However, such quali- tial. McHenry (1992, 1994a,b) provides data sug-
fiers need to placed in context. Compared to Homo, gesting that body mass dimorphism in early homin-
chimpanzees have large canines and substantial ca- ids ranged from comparable to a chimpanzee in
nine dimorphism. But compared to most other pri- Australopithecus robustus, to quite gorilla-like in A.
mates, chimpanzee canines are relatively small in boisei (Plavcan and van Schaik, 1997a). Interest-
both males and females, and canine dimorphism is ingly, the data of McHenry (1992, 1994a,b) suggest
minimal. Hence, the perspective of the viewer needs that Homo erectus, considered as a single species,
to be specified. Using a model of living primates, could have shown substantial body size dimorphism.
most hominids (with the possible exception of A. However, if traditional H. erectus is split into H.
anamensis) had small canines and minimal canine erectus sensu stricto and H. ergaster, then the levels
dimorphism. Compared to humans, it appears that of dimorphism are reduced to levels more compara-
earlier hominids had relatively large canines and ble to modern humans. Regardless, analyses of the
greater canine dimorphism than Homo. face and skeletal elements of early hominids all sug-
Ardipithecus ramidus and Australopithecus ana- gest that body mass dimorphism in these animals
mensis, two of the earliest known hominids to date, was substantial (e.g., Leutenegger and Shell, 1987;
are interesting because they apparently had bigger Hartwig-Scherer, 1993; Richmond and Jungers,
canines than later hominids (White et al., 1994; 1995; Lockwood et al., 1996; Aiello and Wood, 1994;
Leakey et al., 1995). While Ardipithecus ramidus Lockwood, 1999).
canines are described as smaller than those of living Sexual dimorphism has long been used as evi-
chimpanzees (White et al., 1994), A. anamensis ca- dence of either monogamy or polygyny in hominids
nines in particular are described by Leakey et al. (Lovejoy, 1981; Foley and Lee, 1989; McHenry,
(1995) as larger than those of A. afarensis, and char- 1994a,b; Plavcan and van Schaik, 1997a). The prob-
acterized by robust roots. Apparently, there is the lem with using dimorphism to infer behavior in
potential that canine dimorphism in A. anamensis early hominids is the unique combination of mini-
may have been substantial. A ratio of largest to mal canine size dimorphism and intense body mass
smallest specimens published by Leakey et al. dimorphism (Plavcan and van Schaik, 1997a). While
(1995) yields a dimorphism of 41% and 28% for the this pattern of dimorphism is shared with living
mandibular mesiodistal and buccolingual dimen- great apes (Leutenegger and Shell, 1987), the mag-
sions, respectively. This is comparable to that seen nitude of the differences is unique (Plavcan and van
in Gorilla gorilla. This would be truly impressive, Schaik, 1997a). In terms of current comparative
and might suggest that reduced canine dimorphism models for the evolution of canine and body mass
J.M. Plavcan] DIMORPHISM IN PRIMATES 49
dimorphism in primates, there is no clear explana- leads us to the conclusion that sexual dimorphism is
tion for the hominid pattern. Small canines and not a simple function of differential male reproduc-
canine dimorphism imply a lack of male-male com- tive success, but also of pressures on males for dis-
petition, while the strong body mass dimorphism is play, of the interaction between the utility of differ-
consistent with intense male-male competition ent traits as weapons and different fighting
(Plavcan and van Schaik, 1997a). Greenfield (1992a) strategies at different sizes and in different habi-
provides a detailed evaluation of theories for canine tats, and of female counterstrategies against male
reduction in hominids, and concludes that none suf- domination of mating patterns. Dimorphism is also
ficiently explains the phenomenon. The most popu- a function of different developmental pathways, all
lar explanation is that hand-held weapons sup- of which can be affected by different selective pres-
planted the use of the canine teeth in male-male sures throughout an animals entire life-history. Un-
competition (Brace, 1972). However, canine reduc- derstanding these pathways and the selective forces
tion predates the appearance of tools in the fossil that mold them gives profound insights into the
record by millions of years, and fails to explain why evolution of dimorphism. Finally, the fossil record
canines would still not be useful (Plavcan and van teaches us that our extant models do not embrace
Schaik, 1997a). It could be that large male size is the full range of the expression of sexual dimor-
maintained for some other reason apart from sexual phism in primates. Models based on living species
selection, that female choice favored large males, must pass the test of being able to explain the full
that large male size is retained in early hominids range of dimorphism in all primates, including those
through a time lag in its response to a relaxation of from the past.
the selection for large male size, or that there was In spite of all this, there are still very large gaps in
selection for early maturation in females. None of our understanding of the evolution of sexual dimor-
these hypotheses can readily be tested with current phism. Comparative behavioral-ecological models
data from the fossil record. The important point is are far from perfect, and are in constant need of
that the pattern of dimorphism is unique, and that updating. Comparative paternity data alone would
there are a number of reasonable hypotheses to ex- be immensely valuable in identifying and testing
plain it (Plavcan and van Schaik, 1997a), none of different models of the selective basis for dimor-
which can be certainly excluded. Hence, while our phism in primates. Current genetic techniques have
understanding of the evolution of dimorphism in finally made this possible, but as of yet we have no
primates has increased dramatically, the evolution comparative database adequate to this task. Studies
of dimorphism in our own lineage remains an in- on the ontogeny of dimorphism have only just begun.
triguing puzzle. Broadly based comparative patterns of dimorphism
CONCLUSIONS are only now being carefully documented and scru-
tinized. Models of functional and biomechanical con-
This essay provides a brief survey of sexual dimor- straints that could give rise to different patterns of
phism in primates: its expression, the causes of its dimorphism have not been adequately explored.
evolution, and a brief documentation of its presence Hopefully, the future will see an increasing recogni-
in the fossil record. Sexual dimorphism as a phe- tion of the wealth of information on primate evolu-
nomenon is widely familiar. There is even today a tion that can be gleaned from understanding sexual
strong tendency to view dimorphism as a unitary dimorphism.
character that evolves as a simple consequence of
sexual selection. Hopefully this survey has given the ACKNOWLEDGMENTS
reader a sense of the complexity of the phenomenon. I thank the many people who have discussed this
There is wide variation in the expression of sexual topic with me (and critically reviewed my papers)
dimorphism among primates, both in its magnitude over the years, especially Rich Kay, Carel van
and in its pattern. Underlying this variety is a pleth- Schaik, Steve Leigh, Tom Masterson, Mike Lague,
ora of mechanisms that cause or influence the ex- Charlie Nunn, Jay Kelley, Peter Kappeler, Sue
pression and evolution of sexual dimorphism. There Ford, Bernard Wood, Bill Kimbel, Dana Cope, Patri-
is a rich history of comparative studies of sexual cia Vinyard, Gene Albrecht, Rebecca German, Ken
dimorphism, through which ideas have slowly Glander, John Fleagle, Elwyn Simons, Charlie Lock-
changed as students of the topic have realized the wood, Callum Ross, Bill Jungers, Scott McGraw,
subtle difficulties associated with testing the sexual Mike Peirera, Pat Wright, Matt Cartmill, Matt Ra-
selection hypothesis. There has been enormous vosa, Greg Gunnell, Phil Gingerich, Walter Leu-
progress in understanding that sexual dimorphism tenegger, Paul OHiggins, and Richard Smith. I also
is a function of selective pressures on both male and thank the many curators and their staffs at muse-
female traits, and that a complete model of the evo- ums throughout the US, Europe, and South Africa
lution of dimorphism must describe the mechanisms who have been so generous over the years in helping
affecting both males and females. It is now apparent me study the material in their care. Kamla Ahluwa-
that sexual selection, mating systems, and esti- lia kindly reviewed a draft of this manuscript. I
mates of the frequency and intensity of male-male thank Chris Ruff and two anonymous reviewers for
competition do not measure the same thing. This thoughtful comments that greatly improved the
50 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
manuscript. Chris Ruff is a very patient editor. This Demment MW. 1983. Feeding ecology and the evolution of body
paper was partly supported by NSF SBR 9616671. size in baboons. Afr J Ecol 21:219 233.
DeVore I, Washburn SL. 1963. Baboon ecology and human evo-
lution. In: Howell FC, Bourliere F, editors. African ecology and
LITERATURE CITED human evolution. Chicago: Aldine. p 335367.
Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer SR, van den
Aiello LC, Wood BA. 1994. Cranial variables as predictors of Bussche R. 2001. Major-histocompatibility-complex-associated
hominine body mass. Am J Phys Anthropol 95:409 426. variation in secondary sexual traits of white-tailed deer
Alba DM, Moya-Sola S, Kohler M. 2001. Canine reduction in the (Odocoileus virginianus): evidence for good-genes advertise-
Miocene hominoid Oreopithecus bambolii: behavioural and evo- ment. Evolution 55:616 625.
lutionary implications. J Hum Evol 40:116. Dixson AF. 1987. Observations of the evolution of the genitalia
Anderson RW Jr. 1981. Sexual dimorphism in the cranium of and copulatory behaviour in male primates. J Zool Lond 213:
Cercopithecus aethiops. J Hum Evol 10:311317. 423 443.
Anderson RW Jr. 1982. Sexual dimorphism in the cranium of Dixson AF. 1997. Sexual selection and evolution of the seminal
Cercocebus albigena. J Hum Evol 10:143150.
vesicles in primates. Folia Primatol (Basel) 69:300 306.
Andersson M. 1994. Sexual selection. Princeton: Princeton Uni-
Ely J, Kurland JA. 1989. Spatial autocorrelation, phylogenetic
versity Press.
constraints, and the causes of sexual dimorphism in primates.
Bonis L, Koufos GD. 2001. Phylogenetic relationships of Ouran-
Int J Primatol 10:151171.
opithecus macedoniensis (Mammalia, Primates, Hominoidea,
Emlen ST, Oring T. 1977. Ecology, sexual selection, and the
Hominidae) of the late Miocene deposits of Central Macedonia
evolution of mating systems. Science 191:215233.
(Greece). In: Bonis L, Koufos GD, Andrews P, editors. Phylog-
Fairbairn DJ. 1897. Allometry for sexual size dimorphism: pat-
eny of the neogene hominoid primates of Eurasia. Cambridge,
tern and process in the coevolution of body size in males and
UK: Cambridge University Press. p 254 268.
females. Annu Rev Ecol Syst 28:659 687.
Brace CL. 1972. Sexual dimorphism in human evolution. Yrbk
Fedigan L, Fedigan LM. 1988. Cercopithecus aethiops: a review of
Phys Anthropol 16:31 49.
field studies. In: Gautier-Hion A, Bourliere F, Gautier JP, ed-
Brennan EJ. 1985. De Brazzas monkeys (Cercopithecus neglec-
itors. A primate radiation: evolutionary biology of the African
tus) in Kenya: census, distribution and conservation. Am J
Primatol 8:269 277. guenons. Cambridge: Cambridge University Press. p 389 411.
Cheverud JM, Dow MM, Leutenegger W. 1985. The quantitative Fisher RA. 1930. The genetical theory of natural selection. Ox-
assessment of phylogenetic constraints in comparative analy- ford: Clarendon.
sis: sexual dimorphism in body weight among primates. Evo- Fleagle JG. 1999. Primate adaptation and evolution, 2nd ed. New
lution 38:13351351. York: Academic Press.
Clutton-Brock TH. 1985. Size, sexual dimorphism, and polygyny Fleagle JG, Kay RF, Simons EL. 1980. Sexual dimorphism in
in primates. In: Jungers WL, editor. Size and scaling in primate early anthropoids. Nature 287:328 330.
biology. New York: Plenum Press. p 51 60. Foley RA, Lee PC. 1989. Finite social space, evolutionary path-
Clutton-Brock TH, Harvey PH, Rudder B. 1977. Sexual dimor- ways, and reconstructing hominid behavior. Science 243:901
phism, socionomic sex ratio and body weight in primates. Na- 906.
ture 269:191195. Fooden J. 1980. Classification and distribution of living macaques
Cochard LR. 1985. Ontogenetic allometry of the skull and denti- (Macaca Lacepede 1799). In: Lindburg DG, editor. The ma-
tion of the rhesus monkey (Macaca mulatta). In: Jungers WL, caques: studies in ecology, behavior, and evolution. New York:
editor. Size and scaling in primate biology. New York: Plenum Van Nostrand Reinhold Co. p 19.
Press. p 231256. Ford SM. 1994. Evolution of sexual dimorphism in body weight in
Cole TM, Smith FH. 1987. An odontometric assessment of vari- platyrrhines. Am J Primatol 34:221224.
ability in Australopithecus afarensis. J Hum Evol 3:221234. Frayer DW. 1980. Sexual dimorphism and cultural evolution in
Cope DA. 1993. Measures of variation as indicators of multiple the late Pleistocene and Holocene of Europe. J Hum Evol
taxa in samples of sympatric Cercopithecus species. In: Kimbel 9:399 415.
WH, Martin LB, editors. Species, species concepts, and primate Garn SM, Kerewsky RS, Swindler DR. 1966. Canine field in
evolution. New York: Plenum Press. p 211237. sexual dimorphism of tooth size. Nature 212:15011502.
Cope DA, Lacy MG. 1992. Falsification of a single species hypoth- Gaulin SJC, Sailer LD. 1984. Sexual dimorphism in weight
esis using the coefficient of variation: a simulation approach. among primates: the relative impact of allometry and sexual
Am J Phys Anthropol 89:359 378. selection. Int J Primatol 5:515535.
Cope DA, Lacy MG. 1994. Testing single species hypotheses using Gautier-Hion A, Gautier JP. 1985. Sexual dimorphism, social
the combined referent CV: applications to fossil hominoid den- units and ecology among sympatric forest guenons. In: Gues-
tal samples. Am J Phys Anthropol [Suppl] 16:71. quiere J, Martin RD, Newcombe F, editors. Human sexual
Corner BD, Richtsmeier JT. 1991. Morphometric analysis of dimorphism. London: Taylor and Francis. p 6177.
craniofacial growth in Cebus apella. Am J Phys Anthropol Gingerich PD. 1981. Cranial morphology and adaptations in Eo-
84:323342. cene Adapidae. I. Sexual dimorphism in Adapis magnus and
Corner BD, Richtsmeier JT. 1992. Cranial growth in the squirrel Adapis parisiensis. Am J Phys Anthropol 56:217234.
monkey (Saimiri sciureus): a quantitative analysis using three- Gingerich PD. 1995. Sexual dimorphism in earliest Eocene Can-
dimensional coordinate data. Am J Phys Anthropol 87:67 82. tius torresi (Mammalia, Primates, Adapoidea). Contrib Mus
Corner BD, Richtsmeier JT. 1993. Cranial growth and growth Paleontol Univ Mich 29:185199.
dimorphism in Ateles geoffroyi. Am J Phys Anthropol 92:371 Gingerich PD, Schoeninger MJ. 1979. Patterns of tooth size vari-
394. ability in the dentition of primates. Am J Phys Anthropol
Covert HH, Williams BA. 1994. Recent recovered specimens of 51:457 466.
North American Eocene omomyids and adapids and their bear- Godfrey LR, Lyon SK, Sutherland MR. 1993. Sexual dimorphism
ing on debates about anthropoid origins. In: Fleagle JG, Kay in large-bodied primates: the case of the subfossil lemurs. Am J
RF, editors. Anthropoid origins. New York: Plenum Press. p Phys Anthropol 90:315334.
29 54. Greenfield LO. 1992a. Origin of the human canine: a new solution
Crook JH. 1972. Sexual selection, dimorphism, and social orga- to an old enigma. Yrbk Phys Anthropol 35:153185.
nization in the primates. In: Campbell B, editor. Sexual selec- Greenfield LO. 1992b. Relative canine size, behavior, and diet in
tion and the descent of man 18711971. Chicago: Aldine. p male ceboids. J Hum Evol 23:469 480.
231281. Greenfield LO. 1996. Correlated response of homologous charac-
Darwin C. 1871. The descent of man, and selection in relation to teristics in the anthropoid anterior dentition. J Hum Evol 31:
sex. London: J. Murray. 119.
J.M. Plavcan] DIMORPHISM IN PRIMATES 51
Greenfield LO. 1998. Canine tip wear in male and female anthro- Kimbel WL, White TD. 1988. Variation, sexual dimorphism and
poids. Am J Phys Anthropol 107:8796. the taxonomy of Australopithecus. In: Grine FE, editor. Evolu-
Greenfield LO, Washburn A. 1991. Polymorphic aspects of male tionary history of the robust australopithecines. New York:
anthropoid canines. Am J Phys Anthropol 84:1734. Aldine de Gruyter. p 175192.
Greenfield LO, Washburn A. 1992. Polymorphic aspects of male Kinzey WG. 1992. Dietary and dental adaptations in the Pithe-
anthropoid honing premolars. Am J Phys Anthropol 87:173 ciinae. Am J Phys Anthropol 88:499 514.
186. Kramer A, Donnelly SM, Kidder JH, Ousley SD, Olah SM. 1995.
Gustafsson JA. 1994. Regulation of sexual dimorphism in rat Craniometric variation in large-bodied hominoids: testing the
liver. In: Short RV, Balaban E, editors. The differences between single-species hypothesis for Homo habilis. J Hum Evol 29:
the sexes. Cambridge: Cambridge University Press. p 231241. 443 462.
Harcourt AH. 1995. Sexual selection and sperm competition in Krishtalka L, Stucky RK, Beard KC. 1991. The earliest fossil
primates: what are male genitalia good for? Evol Anthropol evidence for sexual dimorphism in primates. Proc Natl Acad Sci
4:121129. USA 87:52235226.
Harcourt AH, Gardiner J. 1994. Sexual selection and genital Lague MR. 2000. Patterns of sexual dimorphism in the joint
anatomy of male primates. Proc R Soc Lond [Biol] 255:4753. surfaces of the elbow and knee of catarrhine primates. Ph.D.
Hartwig-Scherer S. 1993. Body weight prediction in early homi- dissertation, State University of New York at Stony Brook.
nids: towards a taxon-independent approach. Am J Phys An- Lande R. 1980. Sexual dimorphism, sexual selection, and adap-
thropol 92:1736. tation in polygenic characters. Evolution 33:292305.
Harvey PH, Kavanagh M, Clutton-Brock TH. 1978. Sexual dimor- Leakey M, Walker A. 1997. Afropithecus function and phylogeny.
phism in primate teeth. J Zool Lond 186:474 485. In: Begun DR, Ward CV, Rose MD, editors. Function, phylog-
Hayes VJ, Freedman L, Oxnard CE. 1995. The differential ex- eny, and fossils: Miocene hominoid evolution and adaptations.
pression of dental sexual dimorphism in subspecies of Colobus New York: Plenum. p 225239.
guereza. Int J Primatol 16:971996. Leakey MG, Feibel CS, McDougall I, Walker A. 1995. New four-
Hershkovitz P. 1977. Living New World monkeys (Platyrrhini). million-year-old hominid species from Kanapoi and Allia Bay,
Volume 1. Chicago: University of Chicago Press. Kenya. Nature 376:565571.
Jacobs GH. 1994. Variations in primate color vision: mechanisms Le Gros Clark WE. 1971. The antecedents of man. New York:
and utility. Evol Anthropol 3:196 205. Quadrangle Books.
Janson CH, van Schaik CP. 1993. Ecological risk aversion in Leigh SR. 1992. Patterns of variation in the ontogeny of primate
juvenile primates: slow and steady wins the race. In: Pereira body size dimorphism. J Hum Evol 23:2750.
ME, Fairbanks LA, editors. Juvenile primates. New York: Ox- Leigh SR. 1995a. Ontogeny and the evolution of body size dimor-
ford University Press. p 5774. phism in primates. Anthropologie 33:1728.
Jones AL, Degusta D, Turner SP, Campbell J, Milton K. 2000. Leigh SR. 1995b. Socioecology and the ontogeny of sexual size
Craniometric variation in a population of mantled howler mon- dimorphism in anthropoid primates. Am J Phys Anthropol
keys (Alouatta palliata): evidence of size selection in females 97:339 356.
and growth in dentally mature males. Am J Phys Anthropol Leigh SR, Cheverud JM. 1991. Sexual dimorphism in the baboon
113:411 434. facial skull. Am J Phys Anthropol 84:193208.
Kappeler PM. 1990. The evolution of sexual size dimorphism in Leigh SR, Shea BT. 1995. Ontogeny and the evolution of adult
prosimian primates. Am J Primatol 21:201214. body size dimorphism in apes. Am J Primatol 36:37 60.
Kappeler PM. 1991. Patterns of sexual dimorphism in body Leigh SR, Terranova CJ. 1998. Comparative perspectives on bi-
weight among prosimian primates. Folia Primatol (Basel) 57: maturism, ontogeny, and dimorphism in lemurid primates. Int
132146. J Primatol 19:723749.
Kappeler PM. 1996. Intrasexual selection and phylogenetic con- Leutenegger W, Cheverud JM. 1982. Correlates of sexual dimor-
straints in the evolution of sexual canine dimorphism in strep- phism in primates: ecological and size variables. Int J Primatol
sirrhine primates. J Evol Biol 9:43 65. 3:387 402.
Kappeler PM. 1999. Primate socioecology: new insights from Leutenegger W, Cheverud JM. 1985. Sexual dimorphism in pri-
males. Naturwissenschaften 85:18 29. mates: the effects of size. In: Jungers WL, editor. Size and
Kay RF, Plavcan JM, Glander KE, Wright PC. 1988. Sexual scaling in primate biology. New York: Plenum Press. p 3350.
selection and canine dimorphism in New World monkeys. Am J Leutenegger W, Kelly JT. 1977. Relationship of sexual dimor-
Phys Anthropol 77:385397. phism in canine size and body size to social, behavioral and
Kelley J. 1986. Species recognition and sexual dimorphism in ecological correlates in anthropoid primates. Primates 18:117
Proconsul and Rangwapithecus. J Hum Evol 15:461 495. 136.
Kelley J. 1989. Behavioral implications of sexual dimorphism in Leutenegger W, Larson S. 1985. Sexual dimorphism in the post-
Australopithecus afarensis. Am J Phys Anthropol 78:251. cranial skeleton of New World primates. Folia Primatol (Basel)
Kelley J. 1993. Taxonomic implications of sexual dimorphism in 44:8295.
Lufengpithecus. In: Kimbel WH, Martin LB, editors. Species, Leutenegger W, Lubach G. 1987. Sexual dimorphism, mating
species concepts, and primate evolution. New York: Plenum system, and the effect of phylogeny in De Brazzas monkey
Press. p 429 458. (Cercopithecus neglectus). Am J Primatol 13:171179.
Kelley J. 1995a. Sex determination in Miocene catarrhine pri- Leutenegger W, Masterson TJ. 1989a. The ontogeny of sexual
mates. Am J Phys Anthropol 96:391 417. dimorphism in the cranium of Bornean orang-utans (Pongo
Kelley J. 1995b. Sexual dimorphism in canine shape among ex- pygmaeus pygmaeus): I. Univariate analysis. Z Morphol An-
tant great apes. Am J Phys Anthropol 96:365389. thropol 78:114.
Kelley J. 2001. Phylogeny and sexually dimorphic characters: Leutenegger W, Masterson TJ. 1989b. The ontogeny of sexual
canine reduction in Ouranopithecus. In: Bonis L, Koufos GD, dimorphism in the cranium of Bornean orang-utans (Pongo
Andrews P, editors. Phylogeny of the neogene hominoid pri- pygmaeus pygmaeus): II. Allometry and heterochrony. Z Mor-
mates of Eurasia. Cambridge: Cambridge University Press. p phol Anthropol 78:1524.
269 283. Leutenegger W, Shell B. 1987. Variability and sexual dimorphism
Kelley J, Etler D. 1989. Hominoid dental variability and species in canine size in Australopithecus and extant hominoids. J
number at the late Miocene site of Lufeng, China. Am J Pri- Hum Evol 16:359 367.
matol 18:1534. Lieberman SS, Gelvin BR, Oxnard CE. 1985. Dental sexual di-
Kelley J, Plavcan JM. 1998. A simulation test of hominoid species morphisms in some extant hominoids and ramapithecines from
number at Lufeng, China: implications for the use of the coef- China: a quantitative approach. Am J Primatol 9:305326.
ficient of variation in paleotaxonomy. J Hum Evol 35:577596. Lindenfors P, Tullberg BS. 1998. Phylogenetic analysis of pri-
Kelley J, Xu Q. 1991. Extreme sexual dimorphism in a Miocene mate size evolution: the consequences of sexual selection. Biol J
hominoid. Nature 352:151153. Linn Soc 64:413 447.
52 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
Lockwood CA. 1999. Sexual dimorphism in the face of Australo- Plavcan JM. 1993a. Canine size and shape in male anthropoid
pithecus africanus. J Hum Evol 31:537548. primates. Am J Phys Anthropol 92:201216.
Lockwood CA, Richmond BG, Jungers WL, Kimbel WH. 1996. Plavcan JM. 1993b. Catarrhine dental variability and species
Randomization procedures and sexual dimorphism in Austra- recognition in fossils. In: Kimbel WH, Martin LB, editors. Spe-
lopithecus afarensis. J Hum Evol 31:537548. cies, species concepts, and primate evolution. New York: Ple-
Lovejoy CO. 1981. The origin of man. Science 211:341350. num Press. p 239 263.
Lucas PW. 1981. An analysis of canine size and jaw shape in some Plavcan JM. 1998. Correlated response, competition, and female
Old and New World non-human primates. J Zool Lond 195: canine size in primates. Am J Phys Anthropol 107:401 416.
437 448. Plavcan JM. 1999. Mating systems, intrasexual competition and
Lucas PW, Corlett RT, Luke DA. 1986. Sexual dimorphism in sexual dimorphism in primates. In: Lee PC, editor. Compara-
tooth size in anthropoids. Hum Evol 1:2339. tive primate socioecology. Cambridge: Cambridge University
Martin L. 1991. Teeth, sex, and species. Nature 352:111112. Press. p 241269.
Martin RD, Willner LA, Dettling A. 1994. The evolution of sexual Plavcan JM. 2000a. Inferring social behavior from sexual dimor-
size dimorphism in primates. In: Short RV, Balaban E, editors. phism in the fossil record. J Hum Evol 39:327344.
The differences between the sexes. Cambridge: Cambridge Uni- Plavcan JM. 2000b. Variance dimorphism in primates. Am J Phys
versity Press. p 159 200. Anthropol [Suppl] 30:251.
Masterson TJ. 1997. Sexual dimorphism and interspecific cranial Plavcan JM. n.d. Taxonomic variation in the patterns of cranio-
form in two capuchin species: Cebus albifrons and C. apella. facial dimorphism in primates. J Hum Evol (in press).
Am J Phys Anthropol 104:487512. Plavcan JM, Cope DA. 2001. Metric variation and species recog-
Masterson TJ, Hartwig WC. 1998. Degrees of sexual dimorphism nition in the fossil record. Evol Anthropol (in press).
in Cebus and other New World monkeys. Am J Phys Anthropol Plavcan JM, Kay RF. 1988. Sexual dimorphism and dental vari-
107:243256. ability in platyrrhine primates. Int J Primatol 9:169 178.
Masterson TJ, Leutenegger W. 1990. The ontogeny of sexual Plavcan JM, Kelley J. 1996. Evaluating the dual selection hy-
dimorphism in the cranium of Bornean orang-utans (Pongo pothesis of canine reduction. Am J Phys Anthropol 99:379 387.
pygmaeus pygmaeus) as detected by principal-components Plavcan JM, van Schaik CP. 1992. Intrasexual competition and
analysis. Int J Primatol 11:517539. canine dimorphism in anthropoid primates. Am J Phys An-
McHenry HM. 1992. Body size and proportions in early hominids. thropol 87:461 477.
Am J Phys Anthropol 87:407 431. Plavcan JM, van Schaik CP. 1994. Canine dimorphism. Evol
McHenry HM. 1994a. Behavioral ecological implications of early Anthropol 2:208 214.
hominid body size. J Hum Evol 27:77 87. Plavcan JM, van Schaik CP. 1997a. Interpreting hominid behav-
McHenry HM. 1994b. Sexual dimorphism in fossil hominids and ior on the basis of sexual dimorphism. J Hum Evol 32:345374.
its sociological implications. In: Shennan S, Steele J, editors. Plavcan JM, van Schaik CP. 1997b. Intrasexual competition and
Power, sex and tradiation: the archeology of human ancestry.
body weight dimorphism in anthropoid primates. Am J Phys
London: Routledge and Kegan Paul. p 91109.
Anthropol 103:37 68.
Miller JMA. 1991. Does brain size variability provide evidence of
Plavcan JM, van Schaik CP, Kappeler PM. 1995. Competition,
multiple species in Homo habilis? Am J Phys Anthropol 84:
coalitions and canine size in primates. J Hum Evol 28:245276.
385398.
Pope TR. 2000. Reproductive success increases with degree of
Miller JMA. 2000. Craniofacial variation in Homo habilis: an
kinship in cooperative coalitions of female red howler monkeys
analysis of the evidence for multiple species. Am J Phys An-
(Alouatta seniculus). Behav Ecol Sociobiol 48:253267.
thropol 112:103128.
Ravosa MJ. 1990. Functional assessment of subfamily variation
Milton K. 1985. Multimale mating and the absence of canine
in maxillomandibular morphology among Old World monkeys.
tooth dimorphism in woolly spider monkeys (Brachyteles arach-
noides). Am J Phys Anthropol 68:519 523. Am J Phys Anthropol 82:199 212.
Mitani J, Gros-Louis J, Richards AF. 1996. Sexual dimorphism, Ravosa MJ. 1991. The ontogeny of cranial sexual dimorphism in
the operational sex ratio, and the intensity of male competition two Old World monkeys: Macaca fascicularis (Cercopithecinae)
in polygynous primates. Am Nat 147:966 980. and Nasalis larvatus (Colobinae). Int J Primatol 12:403 426.
Napier PH. 1981. Catalogue of primates in the British Museum Ravosa MJ, Ross CF. 1994. Craniodental allometry and hetero-
(Natural History) and elsewhere in the British Isles. Part II: chrony in two howler monkeys: Alouatta seniculus and A. pal-
family Cercopithecidae, subfamily Cercopithecinae. London: liata. Am J Primatol 33:277299.
British Museum (Natural History). Reiss MJ. 1986. Sexual dimorphism in body size: are larger spe-
Napier PH. 1985. Catalogue of primates in the British Museum cies more dimorphic? J Theor Biol 121:163172.
(Natural History) and elsewhere in the British Isles. Part III: Rensch B. 1960. Evolution above the species level. New York:
family Cercopithecidae, subfamily Colobinae. London: British Columbia University Press.
Museum (Natural History). Reynolds JD, Harvey PH. 1994. Sexual selection and the evolu-
Nunn CL. 1999. The evolution of exaggerated sexual swellings in tion of sex differences. In: Short RV, Balaban E, editors. The
primates and the graded-signal hypothesis. Anim Behav 58: differences between the sexes. Cambridge: Cambridge Univer-
229 246. sity Press. p 5370.
OHiggins PO, Moore WJ, Johnson DR, McAndrew TJ. 1990. Richmond BG, Jungers WL. 1995. Size variation and sexual di-
Patterns of cranial sexual dimorphism in certain groups of morphism in Australopithecus afarensis and living hominoids.
extant hominoids. J Zool Lond 222:399 420. J Hum Evol 29:229 245.
Oxnard CE. 1987. Fossils, teeth and sex: new perspectives on Richtsmeier JT, Cheverud JM. 1989. Sexual dimorphism of facial
human evolution. Seattle: University of Washington Press. growth in Macaca mulatta and M. fascicularis. Fortschr Zool
Pagel M. 1994. The evolution of conspicuous oestrus advertise- 35:438 440.
ment in Old World monkeys. Anim Behav 47:13331341. Richtsmeier JT, Cheverud JM, Danahey SE, Corner BD, Lele S.
Phillips-Conroy JE, Jolly CJ. 1981. Sexual dimorphism in two 1993. Sexual dimorphism of ontogeny in the crab-eating ma-
subspecies of Ethiopian baboons (Papio hamadryas) and their caque (Macaca fascicularis). J Hum Evol 25:130.
hybrids. Am J Phys Anthropol 56:115129. Ross C, Williams B, Kay RF. 1998. Phylogenetic analysis of an-
Pickford M. 1986. On the origins of body size dimorphism in thropoid relationships. J Hum Evol 35:221306.
primates. In: Pickford M, Chiarelli B, editors. Sexual dimor- Rowell TE, Chism J. 1986. Sexual dimorphism and mating sys-
phism in living and fossil primates. Florence: Il Sedicesimo. p tems: jumping to conclusions. In: Pickford M, Chiarelli B, edi-
7791. tors. Sexual dimorphism in living and fossil primates. Florence:
Plavcan JM. 1990. Sexual dimorphism in the dentition of extant Il Sedicesimo. p 107111.
anthropoid primates. Ph.D. dissertation. Ann Arbor: Univer- Ryan MJ. 1990. Sexual selection, sensory systems and sensory
sity Microfilms. exploitation. Oxf Surv Evol Biol 7:157195.
J.M. Plavcan] DIMORPHISM IN PRIMATES 53
Schwartz GT, Dean MC. 2001. The ontogeny of canine dimor- van Schaik CP, van Noordwijk MA, Nunn CL. 1999. Sex and
phism in extant hominoids. Am J Phys Anthropol 115:269 283. social evolution in primates. In: Lee PC, editor. Comparative
Setchell JM, Dixson AF. 2001. Circannual changes in the second- primate socioecology. Cambridge: Cambridge University Press.
ary sexual adornments of semifree-ranging male and female p 204 240.
mandrills (Mandrillus sphinx). Am J Primatol 53:109 121. Verrell PA. 1992. Primate penile morphologies and social sys-
Shea BT. 1986. Ontogenetic approaches to sexual dimorphism in tems: further evidence for an association. Folia Primatol
anthropoids. J Hum Evol 1:97110. (Basel) 59:114 120.
Simons EL, Plavcan JM, Fleagle JG. 1999. Canine sexual dimor- Watanabe K. 1981. Variation in group composition and popula-
phism in Egyptian Eocene anthropoid primates: Catopithecus tion density of the two sympatric Mentawian leaf-monkeys.
and Proteopithecus. Proc Natl Acad Sci USA 96:2559 2562. Primates 22:145160.
Small MF. 1989. Female choice in nonhuman primates. Yrbk White TD, Folkens PA. 1991. Human osteology. New York: Aca-
Phys Anthropol 32:103127. demic Press.
Smith RJ, Jungers WL. 1997. Body mass in comparative prima- White TD, Suwa G, Asfaw B. 1994. Australopithecus ramidus, a
tology. J Hum Evol 32:523559. new species of early hominid from Aramis, Ethiopia. Nature
Smuts BB, Smuts RW. 1993. Male aggression and sexual coercion 371:306 312.
of females in nonhuman primates and other mammals: evi- Wolpoff MH. 1976. Some aspects of the evolution of early hominid
dence and theoretical implications. Adv St Behav 22:1 63. sexual dimorphism. Curr Anthropol 17:579 606.
Wood BA. 1976. The nature and basis of sexual dimorphism in the
Spencer MA, Hogard R. 2001. Biomechanics of sexual dimor-
primate skeleton. J Zool Lond 180:1534.
phism in the anthropoid masticatory system. Am J Phys An-
Wood B. 1993. Early Homo: how many species? In: Kimbel WH,
thropol [Suppl] 32:141.
Martin LB, editors. Species, species concepts, and primate evo-
Stallmann RR, Froehlich JW. 2000. Primate sexual swellings as
lution. New York: Plenum. p 485522.
coevolved signal systems. Primates 41:116. Wood BA, Xu Q. 1991. Variation in the Lufeng dental remains. J
Stammbach E. 1987. Desert, forest and montane baboons: multi- Hum Evol 20:291311.
level societies. In: Smuts BB, Cheney DL, Seyfarth RM, Wrang- Wood BA, Li Y, Willoughby C. 1991. Intraspecific variation and
ham RW, Struhsaker TT, editors. Primate societies. Chicago: sexual dimorphism in cranial and dental variables among
University of Chicago Press. p 112120. higher primates and their bearing on the hominid fossil record.
Sterk EHM. 1997. Determinants of female dispersal in Thomas J Anat 174:185205.
langurs. Am J Primatol 42:1789 198. Wu R. 1987. A revision of the classification of the Lufeng great
Stern JT, Susman RL. 1983. The locomotor anatomy of Austra- apes. Acta Anthropol Sin 6:265271.
lopithecus afarensis. Am J Phys Anthropol 60:279 317. Wu R, Oxnard CE. 1983a. Ramapithecines from China: evidence
Trivers RL. 1972. Parental investment and sexual selection. In: from tooth dimensions. Nature 306:258 260.
Campbell B, editor. Sexual selection and the descent of man Wu R, Oxnard CE. 1983b. Ramapithecus and Sivapithecus from
18711971. Chicago: Aldine Publishing Co. p 136 179. China: some implications from higher primate evolution. Am J
Turner TR, Anapol F, Jolly CJ. 1994. Body weights of adult vervet Primatol 5:303344.
monkeys (Cercopithecus aethiops) at four sites in Kenya. Folia Zihlman AL. 1985. Australopithecus afarensis: two sexes or two
Primatol (Basel) 63:177179. species? In: Tobias PV, editor. Hominid evolution: past,
Turner TR, Anapol F, Jolly CJ. 1997. Growth, development, and present, and future. New York: Alan R Liss. p 213220.
sexual dimorphism in vervet monkeys (Cercopithecus aethiops) Zingeser MR. 1969. Cercopithecoid canine tooth honing mecha-
at four sites in Kenya. Am J Phys Anthropol 103:19 35. nisms. Am J Phys Anthropol 31:205214.