Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait

Kensuke Okada,Yasukazu Okada,Manmohan D Sharma,Masako Katsuki,Katsuya Kiyose,David J Hosken,Tomokazu Seko,Alastair J Wilson

doi:10.1038/s41467-021-23804-7

Abstract

Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters.

Highlights

Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and how natural selection can halt trait elaboration
Note that the decision to treat the two mass measures as the same trait across the sexes was justified by an absence of significant genotype-by-sex (GxS) interactions in univariate models—a GxS implies sex limited genetic variance is present and can manifest as cross-sex genetic correlations
Multivariate models further confirmed the presence of additive genetic variance (LRT comparison of null model to one with a diagonal genetic matrix; χ24 = 74.96, P < 0.0001), as well as significant among-trait genetic correlation structure (LRT comparison of a model with a diagonal genetic matrix with all genetic correlations are fixed to zero to the full model in which all genetic correlations are estimated; χ26 = 39.02, P < 0.0001)

Summary

Introduction

Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and how natural selection can halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. They demonstrate how natural selection can oppose sexual selection as trait values move beyond their naturally selected optima One potentially important source of natural selection that could affect the evolution of sexually selected traits is predation[1], and many studies have shown predation can seemingly oppose the exaggeration of male sexual characters. While there is ample evidence that predation selects against sexual trait enhancement, there is limited direct experimental verification that this selection causes evolutionary responses in these traits (but see e.g. 26,27)

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