Abstract

BackgroundIntralocus sexual conflict, arising from selection for different alleles at the same locus in males and females, imposes a constraint on sex-specific adaptation. Intralocus sexual conflict can be alleviated by the evolution of sex-limited genetic architectures and phenotypic expression, but pleiotropic constraints may hinder this process. Here, we explored putative intralocus sexual conflict and genetic (co)variance in a poorly understood behavior with near male-limited expression. Same-sex sexual behaviors (SSBs) generally do not conform to classic evolutionary models of adaptation but are common in male animals and have been hypothesized to result from perception errors and selection for high male mating rates. However, perspectives incorporating sex-specific selection on genes shared by males and females to explain the expression and evolution of SSBs have largely been neglected.ResultsWe performed two parallel sex-limited artificial selection experiments on SSB in male and female seed beetles, followed by sex-specific assays of locomotor activity and male sex recognition (two traits hypothesized to be functionally related to SSB) and adult reproductive success (allowing us to assess fitness consequences of genetic variance in SSB and its correlated components). Our experiments reveal both shared and sex-limited genetic variance for SSB. Strikingly, genetically correlated responses in locomotor activity and male sex-recognition were associated with sexually antagonistic fitness effects, but these effects differed qualitatively between male and female selection lines, implicating intralocus sexual conflict at both male- and female-specific genetic components underlying SSB.ConclusionsOur study provides experimental support for the hypothesis that widespread pleiotropy generates pervasive intralocus sexual conflict governing the expression of SSBs, suggesting that SSB in one sex can occur due to the expression of genes that carry benefits in the other sex.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0658-4) contains supplementary material, which is available to authorized users.

Highlights

  • Intralocus sexual conflict, arising from selection for different alleles at the same locus in males and females, imposes a constraint on sex-specific adaptation

  • The sex selected for sex sexual behavior (SSB) tended to suffer a relative decrease in reproductive success whereas the opposite sex instead enjoyed an increase. These results provide experimental evidence suggesting that widespread pleiotropy generates intralocus sexual conflict (IaSC) at SSB loci via correlated behavioral traits, thereby supporting the hypothesis that IaSC can play an important role in the evolution of SSBs

  • Up-selection resulted in substantially higher mounting rate relative to down-selection (F1,12 = 64.0, p < 0.001). This response was stronger in the sex upon which selection had been applied, especially so for assayed females, suggesting both shared and sex-limited genetic variation for the trait (Fig. 1, full summary of statistics in Additional file 1: S3)

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Summary

Introduction

Intralocus sexual conflict, arising from selection for different alleles at the same locus in males and females, imposes a constraint on sex-specific adaptation. Selection for different alleles at the same locus in males and females can engender a genetic tug-of-war between the sexes, known as intralocus sexual conflict (IaSC) [1,2,3,4,5,6], where adaptations in one sex bear costs paid by the other. Such sexually antagonistic (SA) selection can maintain genetic variance in fitness at relatively high levels SSB is common in non-social animals, exemplified by the fact that same-sex mounting make up nearly 50 % of all mounting attempts in many insects [28]

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