The role of developmental plasticity in evolutionary innovation

Abstract

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.

Figure 1.

Environmentally dependent polyphenism in various taxa. (a) The water flea Daphnia longicephala develops protective crests and tail spines in response to its water bug predator, Notonecta. Differences in coat colour and texture are produced in Arctic fox (Vulpes lagopus) in response to seasonal change. (b) When a bluehead wrasse (Thalassoma bifasciatum) male (blue morph) is removed from his harem, a female (yellow morph) will change phenotype completely and become a male. The gaudy commodore, Precis octavis, is seasonally dimorphic. In the wet season, it has an orange wing and in the dry season the wings are bluish purple in colour. Onthophagus nigriventris dung beetles metamorphose as horned major males or hornless sneaker males in response to ample or insufficient larval feeding resources, respectively. (c) The tiger salamander (Ambystoma tigrinum) only metamorphoses if its aquatic environment becomes uninhabitable. Larval nutrition determines major and minor worker development in Pheidole rhea. The morphology of white water-buttercup (Ranunculus aquatilis) leaves depends on their environment. Submerged leaves are branched into 20 or more thread-like segments. Floating or exposed leaves are scalloped.