Rapid evolution of the intersexual genetic correlation for fitness inDrosophila melanogaster

Julie M Collet,Jack Hesketh,Edward H Morrow,Mark S Hill,Max Reuter,Paolo Innocenti,Kevin Fowler,Sara Fuentes

doi:10.1111/evo.12892

Abstract

Sexual antagonism (SA) arises when male and female phenotypes are under opposing selection, yet genetically correlated. Until resolved, antagonism limits evolution toward optimal sex‐specific phenotypes. Despite its importance for sex‐specific adaptation and existing theory, the dynamics of SA resolution are not well understood empirically. Here, we present data from Drosophila melanogaster, compatible with a resolution of SA. We compared two independent replicates of the “LHM” population in which SA had previously been described. Both had been maintained under identical, controlled conditions, and separated for around 200 generations. Although heritabilities of male and female fitness were similar, the intersexual genetic correlation differed significantly, being negative in one replicate (indicating SA) but close to zero in the other. Using population sequencing, we show that phenotypic differences were associated with population divergence in allele frequencies at nonrandom loci across the genome. Large frequency changes were more prevalent in the population without SA and were enriched at loci mapping to genes previously shown to have sexually antagonistic relationships between expression and fitness. Our data suggest that rapid evolution toward SA resolution has occurred in one of the populations and open avenues toward studying the genetics of SA and its resolution.

Highlights

Sexual antagonism (SA) arises when male and female phenotypes are under opposing selection, yet genetically correlated
The combination of genetically correlated male and female phenotypes and divergent selection on the sexes sets the scene for intralocus sexual conflict or sexual antagonism (SA), where some alleles increase the fitness in one sex at the expense of the fitness in the other sex
These results indicate that the fitness variation between genotypes detected in our experiments is overwhelmingly due to genetic differences, rather than the interaction between genotypes and the specific assay and laboratory environments

Summary

Introduction

Sexual antagonism (SA) arises when male and female phenotypes are under opposing selection, yet genetically correlated. Antagonistic genetic variation has been shown to segregate in natural and laboratory populations of a wide range of organisms, including insects (Chippindale et al 2001; Fedorka and Mousseau 2004; Lewis et al 2011; Berg and Maklakov 2012), vertebrates (Brommer et al 2007; Foerster et al 2007; Mainguy et al 2009; Mokkonen et al 2011), and plants (Kohorn 1994; Scotti and Delph 2006; Delph et al 2011) This growing body of evidence demonstrates that the common genetic basis of male and female phenotypes limits the adaptive evolution of sex-specific traits. Sexual antagonism is a powerful agent for the maintenance of genetic variation for fitness (Kidwell et al 1977)

Methods

Results

Conclusion