Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.
If an ancestral stem group repeatedly colonizes similar environments, developmental plasticity specific to that group should consistently give rise to similar phenotypes. Parallel selection on those similar phenotypes could lead to the repeated evolution of characteristic ecotypes, a property common to many adaptive radiations. A key prediction of this "flexible stem" model of adaptive radiation is that patterns of phenotypic divergence in derived groups should mirror patterns of developmental plasticity in their common ancestor. The threespine stickleback radiation provides an excellent opportunity to test this prediction because the marine form is representative of the ancestral stem group, which has repeatedly given rise to several characteristic ecotypes. We examined plasticity of several aspects of shape and trophic morphology in response to diets characteristic of either the derived benthic ecotype or the limnetic ecotype. When marine fish were reared on alternative diets, plasticity of head and mouth shape paralleled phenotypic divergence between the derived ecotypes, supporting the flexible stem model. Benthic and limnetic fish exhibited patterns of plasticity similar to those of the marine population; however, some differences in population means were present, as well as subtle differences in shape plasticity in the benthic population, indicating a role for genetic accommodation in this system.
Two approaches were used to examine the relationship between seed size and typical establishment conditions in woody species of tropical rain forests. First we compared seed masses of 36 mature tropical forest tree species with differing light-gap requirements for establishment. The 14 species that become established beneath a closed canopy or in small gaps were found to have higher mean seed masses than the species that require large gaps. Though species were divided into two types of establishment requirements, plotting the mean seed masses produced a continuous unimodal distribution rather than a bimodal distribution, suggesting that either intermediate establishment conditions are most common in tropical rain forests or that other biotic or abiotic conditions confound the relationship between establishment conditions and seed mass. Second, we compared seed masses of 203 early and late successional woody plants in one Peruvian forest. Seed masses of mature forest species were found to be significantly larger than those of pioneer species, even when the effects of tree height, dispersal syndrome, and growth form were controlled for statistically. Thus, both analyses demonstrated a relationship between large seed size and establishment in shady, stable plant associations. Additional analysis of the Peruvian forest data demonstrated that mammals tend to disperse larger seeds than birds do, trees tend to have larger seeds than vines, and taller plants of a given growth form tend to produce larger seeds than shorter plants of the same growth form.
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