JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 288:95–98 (2000) © 2000 WILEY-LISS, INC. JEZ Mde2008 What Is the Promise of Developmental Evolution? Part I: Why Is Developmental Biology Necessary to Explain Evolutionary Innovations? GÜNTER P. WAGNER* Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520-8106 Some time in the late 1980s my good friend Jim Cheverud, at the time already a prominent quan- titative geneticist, once asked me the innocuous question: “What is developmental evolution more than evolution of development?” To my dismay I was not able to give a convincing answer (not even one that was convincing to me). The mid-1980s were the last years of the “romantic phase” of de- velopmental evolution (Wagner et al., 2000), and those of us interested in the subject expected great conceptual advances from the integration of de- velopment into evolutionary biology. This was af- ter the publication of Gould’s Ontogeny and Phylogeny (’77), Riedl’s Order in Living Organ- isms (’78), and Raff and Kauffman’s Embryos, Genes, and Evolution (’83). At the time, many thought that there would be a major transforma- tion of evolutionary biology ahead of us (see for instance Horder, ’89; Gilbert, ’91; Wake et al., ’91). Just the evolution of development clearly did not fit the bill. Indeed, for evolutionary biology, the molecular genetic revolution in developmental bi- ology is in some respects like the invention of the electron microscope. A new level of biological or- ganization has come within the grasp of science, and this very fact alone invites the comparative study of the features found at that level of de- scription, i.e., the evolution of development. As such, developmental evolution would not be dif- ferent than any other character specific study of variation, like the evolution of DNA sequences or the evolution of morphological characters. This research is clearly important, but it is not the kind of revolution many of my friends and I expected from developmental biology in the early and mid- 1980s. At that time it was therefore not clear whether embryology or developmental biology would be able to play any explanatory role in evo- lutionary biology (see for instance Wallace, ’86). Jim’s question was answered, somewhat late though, at the inaugural meeting of the new divi- Grant sponsor: National Science Foundation; Grant number: IBN- 9905403. *Correspondence to: G.P. Wagner, Yale University, EEB, 165 Pros- pect Street, P.O. Box 208016, New Haven, CT 06520-8106. E-mail: gunter.wagner@yale.edu Received 18 February 2000; Accepted 30 March 2000 1 Although innovation is the most promising area for developmen- tal evolution, it is not the only area in which development plays a crucial role in explaining evolutionary processes. The other main area is that of developmental constraints, i.e., the influence of develop- mental mechanisms on the pattern of heritable phenotypic variation and their influence on the pattern of diversification (Schwenk, ’95). sion of Evolutionary Developmental Biology of the Society of Integrative and Comparative Biology on January 8, 2000, in Atlanta. Several speakers, including the chair of the new division, Rudolph Raff, emphasized that the most promising areas for Developmental Evolution is the explanation of evolutionary innovations and the evolution of body plans. 1 Indeed, the most exciting research in de- velopmental evolution is directly or indirectly aim- ing at these questions, which proved to be out of the reach of the classical population genetics. Why is this the case? Why is it that evolutionary inno- vations eluded the only causal theory of evolution we have, namely population genetics? And what is it about developmental evolution that makes it look more promising? I want to explore this question through the lens of the concept of “explanatory force.” As introduced by Ron Amundson, “force” means the explanatory significance of a (mechanism), as opposed to any alternative mechanism, with respect to the par- ticular character being explained (Amundson, ’89, p 416). The notion of “explanatory force” is thus not about the validity of a mechanism, but rather about the contribution of a particular mechanism relative to others in accounting for a certain phe- nomenon. This approach acknowledges that popu- lation genetics and developmental genetics are not alternative mechanisms of evolution, but that they both contribute to the explanation of phenotypic