Two forms of sexual dimorphism in gene expression in Drosophila melanogaster: their coincidence and evolutionary genetics

Sex differences in gene regulation is a proximate mechanism by which evolution can resolve sexually antagonistic phenotypic selection. One form of differential gene regulation is sex-biased gene expression (SBGE) in which the sexes differ in the amount a gene is expressed. Less attention has been given to sexual dimorphism in isoform usage (SDIU), resulting from sex differences in alternative splicing. Here, we use RNA-seq data from two tissue types (heads and bodies) from 18 genotypes of adult Drosophila melanogaster to investigate SDIU and SBGE. Both forms of expression dimorphism are both much more prevalent in the body than the head. SDIU is less common among sex-biased than unbiased genes in the body, though the opposite pattern occurs in the head. With respect to body expression, we examine associations of SDIU and SBGE with several evolutionary genetic properties. The intersexual genetic correlation in expression (rmf) increases from female-biased to unbiased to male-biased genes but is drastically reduced for genes with extreme male bias. rmf is lower for genes with versus without SDIU, suggesting that genes with SDIU should be able to evolve greater levels of SBGE holding all else equal. SDIU has no detectable effect on relative non-synonymous diversity. In contrast, non-synonymous diversity is elevated for genes with extreme sex-bias (particularly male-bias) but other effects of SBGE are more subtle. SDIU is associated with reduced values of Tajima’s D. After accounting for correlated variables, sex-bias tends to reduce Tajima’s D. Finally, DoS is elevated for genes with SDIU, suggestive of higher rates of adaptive evolution. In contrast, SBGE is not associated with DoS after excluding genes with extreme male-bias (for which DoS is highly elevated). Together, these results show that both SDIU and SBGE are independently and distinctly associated with evolutionary genetic statistics, suggesting that selection acts somewhat differently on these two dimensions of expression dimorphism. Impact Summary Differences in how genes are expressed between the sexes allow males and females to differ, on average, in a variety of morphological, physiological, and behavioural traits. Using fruit fly data, we examine sexual dimorphism in two different forms of gene expression: (i) sex-biased gene expression (SBGE) quantifies sex differences in the total amount of expression from a gene and (ii) sexual dimorphic isoform usage (SDIU) indicates whether the sexes differ in their relative usage of different isoforms (structurally different proteins coded by the same gene). Based on whole body expression data, we find that these two forms of expression dimorphism co-occur at the same genes less often than expected by chance, possibly indicating that they represent alternative solutions to sexually antagonistic selection. A separate analysis indicates that patterns of quantitative genetic variation are more conducive to genes with SDIU evolving sex differences in total expression than those without SDIU. The observation that SBGE and SDIU are negatively associated suggests that genes with SDIU are not under sexually antagonistic selection for expression or that the variants that would allow for greater dimorphism have other negative effects. An analysis of patterns of DNA sequence variation at the population level suggests that genes with SDIU experience more adaptive evolution than those without. There is little evidence that SBGE is associated with adaptation, except for strongly male-biased genes.