Perspective: Evolutionary Developmental Biology and the Problem of Variation

Abstract

Abstract. One of the oldest problems in evolutionary biology remains largely unsolved. Which mutations generate evolutionarily relevant phenotypic variation? What kinds of molecular changes do they entail? What are the phenotypic magnitudes, frequencies of origin, and pleiotropic effects of such mutations? How is the genome constructed to allow the observed abundance of phenotypic diversity? Historically, the neo-Darwinian synthesizers stressed the predominance of micromutations in evolution, whereas others noted the similarities between some dramatic mutations and evolutionary transitions to argue for macromutationism. Arguments on both sides have been biased by misconceptions of the developmental effects of mutations. For example, the traditional view that mutations of important developmental genes always have large pleiotropic effects can now be seen to be a conclusion drawn from observations of a small class of mutations with dramatic effects. It is possible that some mutations, for example, those in cis-regulatory DNA, have few or no pleiotropic effects and may be the predominant source of morphological evolution. In contrast, mutations causing dramatic phenotypic effects, although superficially similar to hypothesized evolutionary transitions, are unlikely to fairly represent the true path of evolution. Recent developmental studies of gene function provide a new way of conceptualizing and studying variation that contrasts with the traditional genetic view that was incorporated into neoDarwinian theory and population genetics. This new approach in developmental biology is as important for microevolutionary studies as the actual results from recent evolutionary developmental studies. In particular, this approach will assist in the task of identifying the specific mutations generating phenotypic variation and elucidating how they alter gene function. These data will provide the current missing link between molecular and phenotypic variation in natural populations.

Parallel genetic origins of pelvic reduction in vertebrates

“…Perhaps we should not be surprised that the same genetic pathways are involved in parallel evolution of similar traits (1), because the finite number of genes required to build a structure during development limits the realm of possible evolutionary changes (61). However, the total numbers of genes involved in pigmentation, trichome patterning, and limb outgrowth and patterning are not small, and changes in many different genes are known to produce similar phenotypes in laboratory mutants.…”

“…For genes with highly restricted expression patterns, either coding or regulatory mutations can generate new phenotypes that are confined to a particular tissue. For genes expressed in multiple tissues, regulatory mutations in highly modular cis-acting control sequences provide a mechanism to avoid pleiotropic effects and confine phenotypic changes to a particular tissue type or body region (9,57,61).…”

The frailty of adaptive hypotheses for the origins of organismal complexity

“…One could even argue that the stringency of natural selection is reduced in complex organisms with behavioral and/or growth-form flexibilities that allow individuals to match their phenotypic capabilities to the local environment. Some of these shortcomings have recently attracted attention, and a scaffold for connecting evolutionary genetics, genomics, and developmental biology is slowly beginning to emerge (59)(60)(61)(62)(63)(64)(65)(66).…”

Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations

“…Consequently, the independent evolution of similar phenotypes is expected to use unique combinations of genes and alleles (2). New populations, however, are often established in novel environments at the edge of an organism's range, and selective pressures faced in these new habitats are often an important causative factor for adaptive radiations (3).…”