Can Modern Evolutionary Theory Explain Macroevolution?

75

genetic or developmental constraints have been so loose as to be negligible in

practice. Identification and characterization of such constraints is now a major area
of interest, thanks in large part to critiques of the “adaptationist program,” and it is
clear that constraints can be very important in biasing the direction of evolution or
preventing adaptation altogether. Still, it remains heuristically valuable to ask what
kind of selection might have impelled such evolution as has occurred, and in many
(perhaps most) cases, it is likely that selection of some form has played a role.
There is little reason to doubt a role for selection in the evolution of features that
clearly have a close and important bearing on fitness.
The reunion of evolutionary and developmental biology, long overdue, is
beginning to fill a major gap in evolutionary theory, the nature of evolutionary
changes in the mapping between genotype and phenotype and the origin of phe-
notypic variation. Before and since the Evolutionary Synthesis, however, some
developmental biologists have sought to minimize the significance of natural
selection, and even of genetics, in evolution and development, by viewing the
physical processes of development, and of biomolecules and cell structures, as
the locus of explanation. But these are proximal explanations of form, neces-
sary but not sufficient for explaining evolution. Proximal physical processes can
constrain form and are clearly involved in the production of new forms, which
cannot exist other than by physical events. But these events cannot explain the
fixation of the new forms in species populations, nor the further honing of such
features into more precise, effective adaptations. All proteins and cell structures
produce effects by physical processes, but genetically based alteration of the pro-
teins and structures alters the processes. Explanation by gene frequency change
and explanation by changes in the material, mechanistic properties of organisms
are complementary; one need not diminish the significance of the other. Natural
selection on genetic variation remains the ultimate explanation of all adaptive
evolution.
A reawakening of a major role of phenotypic plasticity in evolution is being
presented as another challenge to orthodox theory. Most of the phenotypically
plastic traits under discussion appear to be adaptations to environmental heteroge-
neity that have been shaped by natural selection among genetically variable reac-
tion norms. In some cases, part of such a reaction norm (the phenotype evoked by
and adapted to one of the environmental states) has been genetically consolidated
or assimilated. In other cases, a more extreme phenotype, developed as a simple
extension of the ancestral reaction norm, develops in response to a more extreme
state of the environment. Both of these events, viewed only in the immediate con-
text, appear to illustrate “genes as followers” of developmental phenotypic change,
but in a longer historical perspective are seen to emerge as a by-product of a his-
tory of selection on genetic variation. Perhaps plasticity could be viewed as the
leader, and genes as followers, when a plastically produced phenotype is for-
tuitously “preadapted” to a qualitatively novel environment. I suspect this occurs
rarely, but it remains to be seen.
Many or most epigenetic alterations of phenotype can often be viewed as a
form of phenotypic plasticity. The developmental switch is usually adaptive; it
76 D.J. Futuyma

is often genetically variable, and so it presumably evolved by natural selection.

Epigenetic changes that are inherited across generations can be modeled as ordi-
nary mutations, the long-term evolutionary effect of which depends on their stabil-
ity (or, conversely, on the rate of “back-mutation”) and frequency of occurrence.
Their stability seems seldom to extend beyond a dozen generations or so, and no
cases have yet been described in which epigenetic differences are fixed between
different populations. They clearly can affect fitness and may affect immediate,
local adaptation, but any macroevolutionary role has yet to be established. There is
no evidence, to my knowledge, of a Lamarckian spontaneous origin of adaptively
directed “epimutation” arising de novo.
In agreement with some other authors (e.g., Sterelny 2000; Minelli 2010),
I conclude that the developmental phenomena described to date can readily be
encompassed by the broad principles of the Evolutionary Synthesis.
Variation in rates of diversification stems from dynamics of speciation and
extinction, both of which are explicable in microevolutionary terms. Indeed, the
theory of speciation is far advanced, even if still controversial. However, attempts
to build a theory of diversification from speciation theory have only started. The
fairly minimal existing theory of extinction is surely valid, but obtaining the infor-
mation necessary to predict extinction or to explain differences in extinction rates
will be very difficult.
Finally, can microevolution explain macroevolution? It depends on what
“explain” means. Existing theory can provide a plausible account of the history
and causes of most or all evolutionary phenomena. In many but not all cases, it
will be possible to derive some support or counterevidence from data. The degree
of detail of the account will satisfy some, but not others: For example, there may
be evidence of selection on the genes underlying a phenotype, and of the source
and strength of selection, but the developmental events between gene and phe-
notype may be unknown. Opinion will vary on whether or not the explanation is
complete or sufficient in that case. Likewise, if “explanation” requires that evolu-
tion be predictable for more than a few generations, the theory and data of micro-
evolution will provide no more satisfying “explanation” than does physics if it is
required to make long-term predictions of weather. I do not know of any macro-
evolutionary phenomena that are inconsistent with existing evolutionary theory,
any phenomena that would require us to reject one of its principles as simply
false. Nonetheless, the relative importance of many of the factors of evolution is
debatable, and I assume that every part of our explanatory theory is incomplete.
Of course, the Evolutionary Synthesis will be extended, molded, and modified.
But there will not be a Kuhnian “paradigm shift.” Science really does accomplish
something.

Acknowledgments I am grateful to Michael Bell for calling my attention to a passage in The

Origin of Species in which Darwin seems to foreshadow punctuated equilibria, to Alan Love
for enlightening discussion of the relationship of developmental biology to the Evolutionary
Synthesis, and to two anonymous reviewers for suggestions and queries. I wish also to thank
members of the several audiences to whom I have presented some of these thoughts, whose
questions and criticisms have impelled me to learn more and (I hope) to think more carefully.
Can Modern Evolutionary Theory Explain Macroevolution? 77

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