Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Abstract

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.

Evolutionary Consequences of Sex-Specific Selection in Variable Environments: Four Simple Models Reveal Diverse Evolutionary Outcomes

“…In some contexts, evolutionary trajectories become biased toward the interests of one sex at the expense of the other. These new results strengthen the theoretical foundations of emerging empirical research on the interaction between environmental variation and sex-specific selection (see Delph et al 2011;Long et al 2012;Berger et al 2014;Miller and Svensson 2014;De Lisle and Rowe 2017;De Lisle et al 2018;Olito et al 2018) and provide new impetus for diversifying the range of species in which sexual conflict is studied.…”

Understanding the evolution of ecological sex differences: Integrating character displacement and the Darwin-Bateman paradigm

“…), and salamanders ( Notophtalmus spp .) (De Lisle and Rowe ), males and females occupy distinct regions of morphospace, suggesting macroevolutionary adaptive zones (and thus niches) are not equivalent for males and females of these varied groups. The finding of parallel patterns of ecological divergence between the sexes suggests competition alone is unlikely to explain the evolution of sexual dimorphism in these groups.…”

“…Importantly however, such patterns are expected if both ECD and SA selection related to anisogamy jointly shape divergence between the sexes, and combined with direct experimental approaches to elucidating the action of ECD (e.g. De Lisle and Rowe , , ) can strongly implicate a role for multiple causal drivers of SA selection (note, however, that shared patterns of genetic covariance could also contribute to such patterns). Although a large literature on parallel, or convergent, evolution exists, this literature has rarely considered ecological sex differences (Oke et al.…”

Sexual dimorphism in a top predator ( Notophthalmus viridescens ) drives aquatic prey community assembly

“…As a result, sexual dimorphism in the (sub)species studied here ought to have the most modest impact on prey, both because of the relatively subtle differences between the sexes and because they simply spend less time foraging in aquatic environments [39]. We therefore argue that sexual dimorphism can have important consequences for ecological interactions, but the degree to which differences between the sexes structure ecological communities will depend on the species expressing dimorphism, and more broadly the macroevolution of clades [37,39].…”