Post-insemination sexual selection in males indirectly masculinizes the female transcriptome.

Sexual selection drives the evolution of some of the most dramatic phenotypic differences between the sexes. Such sexual dimorphism is so common across multicellular organisms that we often overlook how remarkable it is for shared genetic material to create numerous and complex sex differences. At an evolutionary level, sexual dimorphism furthers the opportunity for sex-specific selection to optimize the fitness of a given sex. As a consequence, sex-specific selection, such as sexual selection, can have an indirect evolutionary response in the other sex due to genetic associations created by the sexes sharing the same genome. This correlated evolutionary response can create sexual conflict by shifting a sex away from their fitness optimum. At the functional level, sexual dimorphism is generated is through sex-specific regulation of gene expression. Bridging the evolutionary response to sexual selection with the evolution of sex-specific gene regulation during post-mating interactions has proved challenging. We previously used experimental evolution to increase male fertility by directly selecting for increased sperm competitive ability. In this study, we examined the effect of this direct selection on males on gene expression patterns in females. Differential gene expression was determined by whether a female was ancestral or evolved generation, indicating that gene expression changes were an evolved response due to indirect selection on females. Significantly differentially expressed genes were downregulated in evolved females. These genes tended to be female-biased in wildtype individuals and located on the X chromosome. The downregulation of X-linked genes suggests expression levels in females equal to or lower than that in males. Together these results indicate a less female-like transcriptome after experimental evolution. This supports a sexual conflict scenario by which direct sexual selection on males indirectly masculinizes the female transcriptome over short evolutionary timescales.