Abstract

Male genitals are highly divergent in animals with internal fertilization. Most studies attempting to explain this diversity have focused on testing the major hypotheses of genital evolution (the lock‐and‐key, pleiotropy, and sexual selection hypotheses), and quantifying the form of selection targeting male genitals has played an important role in this endeavor. However, we currently know far less about selection targeting female genitals or how male and female genitals interact during mating. Here, we use formal selection analysis to show that genital size and shape is subject to strong multivariate stabilizing sexual selection in both sexes of the red flour beetle, Tribolium castaneum. Moreover, we show significant sexual selection on the covariance between the sexes for specific aspects of genital shape suggesting that male and female genitalia also interact to determine the successful transfer of a spermatophore during mating. Our work therefore highlights the important role that both male and female genital morphologies play in determining mating success and that these effects can occur independently, as well as through their interaction. Moreover, it cautions against the overly simplistic view that the sexual selection targeting genital morphology will always be directional in form and restricted primarily to males.

Highlights

  • Male genitals in animals with internal fertilization are widely regarded as being among the most divergent and variable of all morphological structures, to the extent that genital morphology is often used to distinguish between closely related species that are otherwise indistinguishable

  • We show that male and female genital size and shape play an important role in the successful transfer of a spermatophore during mating in the red flour beetle (Tribolium castaneum)

  • This imposes strong sexual selection on male and female genital morphology that is multivariate stabilizing in form, being characterised by a welldefined peak in fitness at intermediate values of genital size and shape in both sexes

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Summary

Introduction

Male genitals in animals with internal fertilization are widely regarded as being among the most divergent and variable of all morphological structures, to the extent that genital morphology is often used to distinguish between closely related species that are otherwise indistinguishable (reviewed in Hosken and Stockley 2004; Simmons 2014). The sexual selection hypothesis proposes that a number of different processes, most notably cryptic female choice for males with genitals that are better able to stimulate them during mating or through sperm competition and/or sexual conflict, all have the potential to drive genital divergence (Eberhard 1985; Hosken and Stockley 2004). Hosken and Stockley 2004; Ah-King et al 2014; Simmons 2014) This is not altogether surprising given the much larger number of studies testing this hypothesis (Ah-King et al 2014) and highlights the need for more empirical studies focussed on the lock-and-key and pleiotropy hypotheses

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