Abstract

Theoretical models of sexual selection predict that both males and females of many species should benefit by selecting their mating partners. However, empirical evidence testing and validating this prediction is scarce. In particular, whereas inbreeding avoidance is expected to induce sexual conflicts, in some cases both partners could benefit by acting in concert and exerting mutual mate choice for non-assortative pairings. We tested this prediction with the gregarious cockroach Blattella germanica (L.). We demonstrated that males and females base their mate choice on different criteria and that choice occurs at different steps during the mating sequence. Males assess their relatedness to females through antennal contacts before deciding to court preferentially non-siblings. Conversely, females biased their choice towards the most vigorously courting males that happened to be non-siblings. This study is the first to demonstrate mutual mate choice leading to close inbreeding avoidance. The fact that outbred pairs were more fertile than inbred pairs strongly supports the adaptive value of this mating system, which includes no “best phenotype” as the quality of two mating partners is primarily linked to their relatedness. We discuss the implications of our results in the light of inbreeding conflict models.

Highlights

  • A fundamental question raised by the evolution of mating systems addresses the role of each sex in mate choice

  • We argue that B. germanica fulfils the three predicted major requirements for the evolution of mutual mate choice as: i) mate quality varies with levels of genetic relatedness between partners; ii) gregariousness facilitates encounters with potential mates and assessment of mate quality; and iii) males invest in long-lasting courtships and costly spermatophores and females invest in costly oothecae

  • Males clearly biased their courting investment towards non-siblings female lures, suggesting male mating preference based on their relatedness to females. As they persistently preferred to court non-sibling partners, even when they were male lures, we can discard the hypothesis of cryptic information transfer from females to males that would influence male decision. This validates the hypothesis of precopulatory mate choice by males and B. germanica can be added to the growing list of species for which male mate selectivity has been reported [15,16,17,18,19,20], [31], [50,51,52]

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Summary

Introduction

A fundamental question raised by the evolution of mating systems addresses the role of each sex in mate choice. This implies understanding the keys used to select mating partners and how and when they are used. A growing number of theoretical models predict that members of both sexes should be selective when they incur similar reproductive costs, resulting in assortative pairings of mate quality [8,9,10,11,12,13,14]. Empirical data testing and validating these predictions remain relatively scarce [15,16,17,18,19,20]

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