Disruptive natural selection predicts divergence between the sexes during adaptive radiation.

Stephen P De Lisle,Locke Rowe

doi:10.1002/ece3.2868

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.

Highlights

The ecological theory of adaptive radiation suggests lineages diverge to exploit ecological opportunity, appealing to evolutionary biologists by simultaneously explaining diversity of species, their phenotypes, and the habitats in which both reside (Schluter, 2000)
The role of this within-species divergence in adaptive radiation becomes especially interesting in the case of sexual dimorphism in ecologically relevant traits, such as body size and feeding morphology, because theory suggests that these ecological sexual dimorphisms can be driven by the same processes of resource competition and niche divergence that are envisioned to be key drivers of ecological speciation during adaptive radiations of genetically independent lineages (Slatkin, 1984)
We have shown that morphological divergence between the sexes across a clade of salamanders has occurred in a combination of head- shape traits that past work (De Lisle & Rowe, 2015a) has shown to be under disruptive, competition-driven natural selection within breeding ponds

Summary

| INTRODUCTION

The ecological theory of adaptive radiation suggests lineages diverge to exploit ecological opportunity, appealing to evolutionary biologists by simultaneously explaining diversity of species, their phenotypes, and the habitats in which both reside (Schluter, 2000). We can make three predictions: if similar processes of resource competition drive evolution of sexual dimorphism across the genus, (1) we expect SA natural selection to align with morphological divergence between the sexes, and (2) the extent of sexual dimorphism to associate with an aquatic life history This prediction can be made on the basis of biomechanical trade-offs between foraging in aquatic (via bidirectional suction) versus terrestrial (via tongue prohesion) habitat (Deban & Wake, 2000; Wake & Deban, 2000); there is an a priori expectation that selection on multivariate feeding morphology would differ fundamentally across these habitats, as reflected in the intermediate feeding morphology that characterizes semiaquatic newts (Deban & Wake, 2000; Heiss, Aerts, & Van Wassenbergh, 2013) and the morphological changes that underlie transitions between these habitats in salamanders and other vertebrates (Schwenk, 2000). Note that this prediction holds regardless of how speciation has proceeded

| MATERIALS AND METHODS

| DISCUSSION

Findings

D SVL Gape Head depth Jaw length