Developmental noise and ecological opportunity across space can release constraints on the evolution of plasticity

Abstract

Phenotypic plasticity is a potentially definitive solution to environment heterogeneity, driving biologists to understand why it is not ubiquitous in nature. While costs and constraints may limit the success of plasticity, we are still far from a complete theory of when these limitations actually proscribe adaptive plasticity. Here I use a simple model of plasticity incorporating developmental noise to explore the competitive and evolutionary relationships of specialist and generalist genotypes spreading across a heterogeneous landscape. Results show that plasticity can arise in the context of specialism, preadapting genotypes to later evolve toward plastic generalism. Developmental noise helps a mutant with imperfect plasticity successfully compete against its ancestor, providing an evolutionary path by which subsequent mutations can refine plasticity toward its optimum. These results address how the complex selection pressures across a heterogeneous environment can help evolution find paths around constraints arising from developmental mechanisms.

Historical and philosophical perspectives on the study of developmental bias

“…In a similar vein, the contributions to this special issue illustrate that the study of developmental bias spans different biological domains (and thus implicates different fields): gene regulation (e.g., Hu et al, ), parthenogenesis (Galis & van Alphen, ), phenotypic plasticity (Draghi, ; Levis & Pfennig, ; Parsons et al, ; Uller et al, ), the morphology of extant and fossil species (Jablonski, ; Jackson, ), brain development (Finlay & Huang, ), symbiosis and interactions involving microbial species (Gilbert, ), development of the vertebrate skeleton (Kavanagh, ), and behavior, learning, and niche construction (Hu et al, ; Laland et al, ), among others. Some of the studies are experimental, some include field work, and others make primarily use of theory and computational simulation (Draghi, ; Hordijk & Altenberg, ). Given this diversity of individual projects and biological fields involved, it would indeed be beneficial to have all the researchers united by a common intellectual identity.…”

“…The term "developmental bias" is clearly preferable over "constraint" because it highlights the generation of positive variation, while also having an edge on "evolvability" by pointing to the production of very distinctive trajectories of phenotypic evolution, which lend support to an explanatory strategy in terms of development (without conflating it with the role of selection). Biases result not only from the organization of gene regulatory networks, but in many cases also from the nature of phenotypic plasticity, so that the interaction between development and an organism's environment has to be part of the explanatory story (Draghi, 2019;Levis & Pfennig, 2019;Parsons et al, 2019;Uller et al, 2019). Although the idea of a developmental mechanism's variational properties is an empirically adequate notion, it again includes any instance of variation.…”

“…Many will argue that an explanation of developmental bias requires more than the study of gene regulatory mechanisms. Indeed, several of the contributions to this special issue investigate cases where phenotypic plasticity (Draghi, 2019;Levis & Pfennig, 2019;Parsons, McWhinnie, Pilakouta, & Walker, 2019;Uller, Feiner, Radersma, Jackson, & Rago, 2019), niche construction (Hu et al, 2019;Laland, Toyokawa, & Oudman, 2019), and symbiosis (Gilbert, 2019) form the basis for biases in phenotypic variation. Generally, phenotypic variation is not only generated by means of mutations, but also by environmental changes, where such environmentally induced variation can matter for evolution (Sultan, 2017;West-Eberhard, 2003).…”

“…Regarding the alternative concept of developmental bias, apart from the relevance of cases from the fossil record, I have highlighted criteria that call for an eco‐devo perspective, which Salazar‐Ciudad's () reliance on “developmental mechanism” could obscure. Biases result not only from the organization of gene regulatory networks, but in many cases also from the nature of phenotypic plasticity, so that the interaction between development and an organism's environment has to be part of the explanatory story (Draghi, ; Levis & Pfennig, ; Parsons et al, ; Uller et al, ). Cases of niche construction and animal learning can lead to biases, in which case organism–environment mutual influences, organism–organism interactions, and animal behavior are part of the “developmental” account (Hu et al, ; Laland et al, ).…”

Biases in the study of developmental bias

“…The resulting possibility of plasticity-led evolution is the subject of five contributions to this issue. These models show not only how plasticity may arise in the context of specialization, but also how developmental noise may help a mutant with imperfect plasticity compete successfully against its ancestor, thereby providing an evolutionary path through which subsequent mutations can refine plasticity toward an optimum (Draghi, 2019). Parsons, McWhinnie, Pilakouta, and Walker (2019) then explore how developmental plasticity may contribute to developmental bias, and how the resulting biased variation may echo past adaptations that reflect the evolutionary history of a lineage, or alternatively, serve to initiate evolution when environments change.…”