Developmental plasticity and the origin of species differences
Abstract
Speciation is the origin of reproductive isolation and divergence between populations, according to the “biological species concept” of Mayr. Studies of reproductive isolation have dominated research on speciation, leaving the origin of species differences relatively poorly understood. Here, I argue that the origin of species differences, and of novel phenotypes in general, involves the reorganization of ancestral phenotypes (developmental recombination) followed by the genetic accommodation of change. Because selection acts on phenotypes, not directly on genotypes or genes, novel traits can originate by environmental induction as well as mutation, then undergo selection and genetic accommodation fueled by standing genetic variation or by subsequent mutation and genetic recombination. Insofar as phenotypic novelties arise from adaptive developmental plasticity, they are not “random” variants, because their initial form reflects adaptive responses with an evolutionary history, even though they are initiated by mutations or novel environmental factors that are random with respect to (future) adaptation. Change in trait frequency involves genetic accommodation of the threshold or liability for expression of a novel trait, a process that follows rather than directs phenotypic change. Contrary to common belief, environmentally initiated novelties may have greater evolutionary potential than mutationally induced ones. Thus, genes are probably more often followers than leaders in evolutionary change. Species differences can originate before reproductive isolation and contribute to the process of speciation itself. Therefore, the genetics of speciation can profit from studies of changes in gene expression as well as changes in gene frequency and genetic isolation.
Footnotes
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↵ * To whom correspondence should be addressed at: Escuela de Biología, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica. E-mail: mjwe{at}sent.com.
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This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Systematics and the Origin of Species: On Ernst Mayr's 100th Anniversary,” held December 16-18, 2004, at the Arnold and Mabel Beckman Center of the National Academies of Science and Engineering in Irvine, CA.
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↵ † The assumption that genetic inputs are more reliable than environmental ones may be further challenged by future research on gene expression. Recent findings suggest that processes like gene transcription, involving small numbers of molecules, are especially subject to randomness and noise (46).
- Copyright © 2005, The National Academy of Sciences
