Plasticity‐led evolution: A survey of developmental mechanisms and empirical tests

Abstract

Recent years have witnessed increased interest in evaluating whetherphenotypic plasticity can precede, facilitate, and possibly even bias adaptive evolution. Despite accumulating evidence for "plasticity-led evolution" (i.e., "PLE"), critical gaps remain, such as: how different developmental mechanisms influence PLE; whether some types of traits and taxa are especially prone to experience PLE; and what studies are needed to drive the field forward. Here, we begin to address these shortcomings by first speculating about how various features of development-modularity, flexible regulation, and exploratory mechanisms-might impact and/or bias whether and how PLE unfolds. We then review and categorize the traits and taxa used to investigate PLE. We do so both to identify systems that may be well-suited for studying developmental mechanisms in a PLE context and to highlight any mismatches between PLE theory and existing empirical tests of this theory. We conclude by providing additional suggestions for future research. Our overarching goal is to stimulate additional work on PLE and thereby evaluate plasticity's role in evolution.

Historical and philosophical perspectives on the study of developmental bias

“…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).…”

Biases in the study of developmental bias

“…Developmental plasticity, and related phenomena such as phenotypic accommodation (the mutual adjustment of multiple traits in response to perturbations) and genetic accommodation (heritable changes in the regulation of an environmentally induced trait) are increasingly considered relevant in the initiation and structuring of phenotypic variation, including the origin of phenotypic novelties (Moczek, 2012). The contribution by Levis and Pfennig (2019), in turn, focuses on the gaps in our knowledge of the mechanisms and consequence of plasticity-led evolution regarding the developmental mechanisms, traits, or taxa most affected by it, and provide suggestions for future research approaches to address these shortcomings. Uller, Feiner, Radersma, Jackson, and Rago (2019) explore how assumptions meant to simplify the starting point for a conceptual framework set the stage for what counts, and what does not, as an evolutionary explanation, and why prevailing idealizations prevent an integration of the role of development in general, and plasticity in particular, in evolutionary theory.…”

Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

“…This is especially true for adaptive plasticity, which we define as a change in a phenotype that occurs in response to a specific environmental signal or cue and that enhances fitness (sensu Stearns, 2014). Clarifying the molecular mechanisms underlying adaptive plasticity is crucial for ultimately understanding its downstream impacts on ecology and evolution (Gilbert & Epel, 2015; Levis & Pfennig, 2020). [NB: We treat plasticity as synonymous/encompassing G × E, because plasticity naturally requires an interaction between an organism's genes and its environment (i.e., purely environmental effects are not biologically plausible), and because natural populations often show variation in plasticity among genotypes or individuals (Falconer & Mackay, 1996; Sultan & Stearns, 2005).…”