Signatures of sexually antagonistic selection in sex-specific dominance of gene expression

In theory, selection that fluctuates across environments can generate net balancing selection if dominance reversal occurs, where alternate alleles are dominant in the environment in which they are favoured. The sexes represent two distinct genetic environments and sexually antagonistic selection may maintain genetic variation through balancing selection whenever the alleles involved in sexually antagonistic selection show sex-specific dominance reversal for fitness. A few recent case studies have shown that such dominance reversals do occur. Sexual dimorphism in gene expression is pervasive and it has been suggested that sexually antagonistic selection is key in the evolution of gene expression. Yet, whether segregating variants in regulatory regions that affect expression show shared or sex-specific dominance effects is unknown. This knowledge-gap is unfortunate, because recent theory predicts that sexually antagonistic selection should favour sex-dependent dominance modification and because sex-specific dominance of variants that affect gene expression could contribute importantly to the maintenance of genetic variation in gene expression and in fitness-related traits. Here, we test for sex-specific dominance in gene expression in an RNA sequencing experiment involving three independent crosses between homozygous lines derived from a single population of the seed beetle Callosobruchus maculatus. In a previous quantitative genetic study, a genome wide signal of dominance-reversal for fitness between the sexes was documented in this population. We found that dominance effects of variants affecting gene expression were only weakly correlated between the sexes, and the expression of several hundred genes showed significant dominance differences between the sexes. Sex-specific dominance was more common in transcripts with sex-biased expression, although significantly so only in one cross. We found no overall relationship between the direction of sex-bias and the direction of dominance. Gene ontology enrichment analyses revealed that transcripts functionally related to phenotypic traits known to be under sexually antagonistic selection in C. maculatus were significantly overrepresented among genes with sex-specific dominance effects, including an enrichment of genes involved in metabolic processes, growth regulation and male courtship. Our results suggest that sex-specific dominance effects of regulatory variants affecting gene expression play an important role in the maintenance of genetic variation in fitness in this species.