Abstract
The evolution of sexual dimorphism is constrained by a shared genome, leading to ‘sexual antagonism’, in which different alleles at given loci are favoured by selection in males and females. Despite its wide taxonomic incidence, we know little about the identity, genomic location, and evolutionary dynamics of antagonistic genetic variants. To address these deficits, we use sex-specific fitness data from 202 fully sequenced hemiclonal Drosophila melanogaster fly lines to perform a genome-wide association study (GWAS) of sexual antagonism. We identify approximately 230 chromosomal clusters of candidate antagonistic single nucleotide polymorphisms (SNPs). In contradiction to classic theory, we find no clear evidence that the X chromosome is a hot spot for sexually antagonistic variation. Characterising antagonistic SNPs functionally, we find a large excess of missense variants but little enrichment in terms of gene function. We also assess the evolutionary persistence of antagonistic variants by examining extant polymorphism in wild D. melanogaster populations and closely related species. Remarkably, antagonistic variants are associated with multiple signatures of balancing selection across the D. melanogaster distribution range and in their sister species D. simulans, indicating widespread and evolutionarily persistent (about 1 million years) genomic constraints on the evolution of sexual dimorphism. Based on our results, we propose that antagonistic variation accumulates because of constraints on the resolution of sexual conflict over protein coding sequences, thus contributing to the long-term maintenance of heritable fitness variation.
Highlights
The divergent reproductive roles of males and females favour different phenotypes [1,2]
We examined the properties of candidate antagonistic polymorphisms, including their genomic distribution across the X chromosome and autosomes, their functional characteristics, the genes in which they occur, and their population genomic dynamics across a number of wild populations of D. melanogaster and two closely related species, D. simulans and D. yakuba
Long-standing genomic constraints on sexual dimorphism in fruit flies genetic variation at antagonistic loci is stably maintained across D. melanogaster populations throughout the species’ distribution range, and across species boundaries into D. simulans. These results demonstrate that the targets of antagonistic selection have been largely conserved for many millennia [50,58,59,60]—and hundreds of thousands of generations—and that a number of antagonistic polymorphisms have arisen and persisted since the speciation event between D. melanogaster and D. simulans, approximately 1 million years ago
Summary
The divergent reproductive roles of males and females favour different phenotypes [1,2] Responses to these selective pressures are constrained by a shared genome, leading to ‘sexual antagonism’, in which different alleles at given loci are favoured in the two sexes [1,3,4,5]. Genome-wide allele frequency differences between males and females have been used to infer sex-specific selection on viability [18], but this approach neglects important reproductive components of fitness, and cannot distinguish between loci with opposing fitness effects in each sex (sexually antagonistic loci) and loci where the strength of sexually concordant selection differs between the sexes. It is essential that we characterise causal antagonistic loci underlying lifetime reproductive success in order to understand the adaptive limits to sexual dimorphism and mechanisms of conflict resolution
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