Commentary: The promise of ecological developmental biology

In a persuasive essay on the promise of developmental evolution, Wagner (2000) argued that this synthetic discipline can make a unique explanatory contribution to evolutionary biology. Identifying developmental and molecular mechanisms and how they have changed at crucial junctures is key to understanding the range of phenotypic possibilities available through evolutionary time, and hence major steps in morphological evolution. Here I discuss a second recently emerged discipline that can profoundly enrich our understanding of the evolutionary process and of biological diversity, as well as of development itself. Ecological development investigates the development of organisms in their natural contexts. This investigation shifts our focus to the immediate interactions between individual organisms and their environments (and to the underlying mechanisms of those interactions). ‘‘Eco-devo’’ thus illuminates the ecological and hence microevolutionary implications of development, providing the critical complement to the macroevolutionary focus of the evolutionary development problematic (Gilbert, 2001). The goal of ecological developmental biology is to include the environment in studying both the developmental causes and the ecological consequences of phenotypic variation. This inclusion of the environment is not a contemporary innovation but rather a restoration of an earlier, more holistic approach to understanding individual development. Early twentieth-century German biologists viewed the genotype as a repertoire of environmentally contingent phenotypic potentialities or ‘‘norm of reaction’’ to the environment, rather than as a rigid developmental blueprint (Sapp, ’87; Sultan, ’87; Stearns, ’89; Sarkar, ’99). Accordingly, every phenotype was understood to represent a genotype -by-environment interaction: the expression of a given genotype under its particular environmental influences. With the growing professional dominance of transmission genetics in studies of heredity (Amundsen, 2001), the adoption by New Synthesis evolutionists of a determinate, strictly Mendelian notion of gene expression (Sultan, ’92), and an increasing focus on ‘‘model’’ organisms chosen specifically to express minimal environmental responses (Bolker, ’95; Gilbert, 2001), the phenotype came to be seen instead as the direct, fixed outcome of the genotype. Accordingly the earlier genotype/ environment paradigm was displaced by purely gene-based models in both developmental and evolutionary biology. Evolutionary biologists such as Schmalhausen and Waddington who took an integrative approach remained outside the mainstream. Neo-Darwinian theory became, in R. A. Fisher’s phrase ‘‘a genetical theory of natural selection’’ that defined evolution as change in allele frequencies rather than in organisms. One clear consequence of this approach, which has dominated evolutionary biology since its origin during the mid-twentieth century, was the exclusion of developmental biology from studies of evolutionary change in populations (Hamburger, ’80; Amundsen, 2001). However, starting in the late 1970’s ecological geneticists and life history theorists sought increasingly to integrate the complexity of environmental response into their understanding of evolutionary processes [e.g., the seminal work of Stearns (’77, ’82); Jain (’79); Gupta and Lewontin (’82); and Scheiner and Goodnight (’84)]. Since that time a considerable body of work in ecological development has emerged, together with insights and approaches that hold the promise of redressing this disjunc-