Mating system manipulation and the evolution of sex-biased gene expression in Drosophila

Abstract

Sex differences in dioecious animals are pervasive and result from gene expression differences. Elevated sexual selection has been predicted to increase the number and expression of male-biased genes, and experimentally imposing monogamy on Drosophila melanogaster has led to a relative feminisation of the transcriptome. Here, we test this hypothesis further by subjecting another polyandrous species, D. pseudoobscura, to 150 generations of experimental monogamy or elevated polyandry. We find that sex-biased genes do change in expression but, contrary to predictions, there is usually masculinisation of the transcriptome under monogamy, although this depends on tissue and sex. We also identify and describe gene expression changes following courtship experience. Courtship often influences gene expression, including patterns in sex-biased gene expression. Our results confirm that mating system manipulation disproportionately influences sex-biased gene expression but show that the direction of change is dynamic and unpredictable.

The microevolutionary response to male-limited X-chromosome evolution inDrosophila melanogasterreflects macroevolutionary patterns

“…Increased sexual conflict has been suggested to induce an overall shift towards the male expression optimum (Hollis et al 2014, Immonen et al 2014, Innocenti et al 2014, Perry et al 2016, and might therefore be expected to parallel the changes seen here as a result of reducing female-specific selection and resolving sexual antagonism (but see Veltsos et al 2017). Evidence for parallel changes was equivocal.…”

“…Replicate population was considered a random factor nested within treatment. In line with other studies of expression changes after experimental evolution (Immonen et al 2014, Veltsos et al 2017), we did not employ a foldchange cutoff since most changes were expected to be relatively small.…”

“…(2014), but there was overrepresentation of genes identified by Immonen et al (2014). Given that changes as a result of alterations of sexual conflict seem to preferentially involve sex-biased genes (Hollis et al 2014, Immonen et al 2014, Innocenti et al 2014, but that the direction of the change is sometimes opposite to the direction of sex-bias (Veltsos et al 2017, Parker et al 2019, it seems likely that any overlap with sexually antagonistic loci is caused by the fact that both phenomena are related to sexual dimorphism, and not because increased sexual conflict resolves antagonism per se.…”

“…Hollis et al 2014), but others do not (e.g. Immonen et al 2014, Veltsos et al 2017. In contrast, studies of sex chromosome evolution are often observational or comparative in nature (e.g.…”

Persistent postmating, prezygotic reproductive isolation between populations

“…Such postcopulatory sexual selection, and its attendant sexual conflict within populations (Andersson, 1994;Andersson & Simmons, 2006;Arnqvist & Rowe, 2002;Gavrilets, 2000), can shape the evolution of intersexual interactions during copulation and fertilization (Bernasconi et al, 2004;Birkhead & Pizzari, 2002;Firman, Gasparini, Manier, & Pizzari, 2017). Rapid evolution of such phenotypes is supported by evidence that genes encoding reproductive tract proteins are among the fastest evolving, showing rapid protein sequence and gene expression evolution (Hollis, Houle, Yan, Kawecki, & Keller, 2014;Perry et al, 2016;Swanson & Vacquier, 2002;Veltsos, Fang, Cossins, Snook, & Ritchie, 2017).…”