The genomic footprint of sexual conflict

Abstract

Genes with sex-biased expression show a number of unique properties and this has been seen as evidence for conflicting selection pressures in males and females, forming a genetic 'tug-of-war' between the sexes. However, we lack studies of taxa where an understanding of conflicting phenotypic selection in the sexes has been linked with studies of genomic signatures of sexual conflict. Here, we provide such a link. We used an insect where sexual conflict is unusually well understood, the seed beetle Callosobruchus maculatus, to test for molecular genetic signals of sexual conflict across genes with varying degrees of sex-bias in expression. We sequenced, assembled and annotated its genome and performed population resequencing of three divergent populations. Sex-biased genes showed increased levels of genetic diversity and bore a remarkably clear footprint of relaxed purifying selection. Yet, segregating genetic variation was also affected by balancing selection in weakly female-biased genes, while male-biased genes showed signs of overall purifying selection. Female-biased genes contributed disproportionally to shared polymorphism across populations, while male-biased genes, male seminal fluid protein genes and sex-linked genes did not. Genes showing genomic signatures consistent with sexual conflict generally matched life-history phenotypes known to experience sexually antagonistic selection in this species. Our results highlight metabolic and reproductive processes, confirming the key role of general life-history traits in sexual conflict.