Sexual selection drives evolution and rapid turnover of male gene expression

Abstract

The profound and pervasive differences in gene expression observed between males and females, and the unique evolutionary properties of these genes in many species, have led to the widespread assumption that they are the product of sexual selection and sexual conflict. However, we still lack a clear understanding of the connection between sexual selection and transcriptional dimorphism, often termed sex-biased gene expression. Moreover, the relative contribution of sexual selection vs. drift in shaping broad patterns of expression, divergence, and polymorphism remains unknown. To assess the role of sexual selection in shaping these patterns, we assembled transcriptomes from an avian clade representing the full range of sexual dimorphism and sexual selection. We use these species to test the links between sexual selection and sex-biased gene expression evolution in a comparative framework. Through ancestral reconstruction of sex bias, we demonstrate a rapid turnover of sex bias across this clade driven by sexual selection and show it to be primarily the result of expression changes in males. We use phylogenetically controlled comparative methods to demonstrate that phenotypic measures of sexual selection predict the proportion of male-biased but not female-biased gene expression. Although male-biased genes show elevated rates of coding sequence evolution, consistent with previous reports in a range of taxa, there is no association between sexual selection and rates of coding sequence evolution, suggesting that expression changes may be more important than coding sequence in sexual selection. Taken together, our results highlight the power of sexual selection to act on gene expression differences and shape genome evolution.sperm competition | sex-biased gene expression | gene expression evolution | sexual dimorphism | sexual conflict N umerous studies across a range of organisms have convergently shown that the majority of variation in overall gene expression is explained by sex (1-6). These sex-biased genes have distinct evolutionary properties, namely they show faster rates of sequence and expression divergence, as well as rapid rates of turnover, broadly consistent with sexual selection (7, 8). The sizable proportion of genes exhibiting sex-biased expression suggests that sexual selection has the potential to shape many aspects of genome biology. Recent studies of intrasexual variation in gene expression differences between males and females of the same species have revealed patterns of overall transcription consistent with the degree of phenotypic sexual dimorphism (9, 10), and experimental manipulation of sex-specific selection affects sex-biased gene expression over short time scales (11-13). These studies together suggest that increasing sexual selection across species should lead to increased turnover in sex-biased gene expression and a greater sexualization of the transcriptome over longer evolutionary timescales.The elevated rates of coding sequence evolution often (14) but not always (15) observed for m...

Sex differences in DNA methylation and expression in zebrafish brain: a test of an extended ‘male sex drive’ hypothesis

“…Not surprisingly, female and male gonads usually differ remarkably in the sets of highly expressed genes [4][5][6][7]. Sex-biased gene expression, although less pronounced than in the gonads, has been also found in many somatic tissues, such as liver, spleen, muscles and brain [4,8,9].…”

Avian transcriptomics: opportunities and challenges

“…Chung et al 2015;Mueller et al 2015). Wright et al (2014) [3] {18, 22, 23}; Harrison et al (2015) [3] {18, 22, 23}; Li et al (2015) [2] {3, 22, 24}; Smith et al (2015) [2] {12, 16}; Wright et al (2015) [3] {18, 22, 23} Anser cygnoides Swan Goose a Harrison et al (2015) [3] {18, 22, 23}; Lu et al (2015) [1, 2] {15}; Tariq et al (2015) [2] {28}; Wright et al (2015) [3] {18, 22, 23}; Chen et al (2017b) [2] {28}; Cao et al (2017) Harrison et al (2015) [3] {18, 22, 23}; Wright et al (2014) [3] {18, 22, 23}; Wright et al (2015) [3] {18, 22, 23} Numida meleagris Helmeted Guineafowl Harrison et al (2015) [3] {18, 22, 23}; Wright et al (2015) [3] {18, 22, 23} Pavo cristatus Indian Peafowl Harrison et al (2015) [3] {18, 22, 23}; Wright et al (2015) [3] {18, 22, 23}…”

“…Common Pheasant Harrison et al (2015) [3] {18, 22, 23}; Wright et al (2015) (Richardson et al 2017). To facilitate future molecular ecology and evolution studies in the European Starling, Richardson et al (2017) characterised the liver transcriptome of this species.…”

The evolution of sex-biased gene expression in Drosophila serrata

“…The fact that these evolutionary patterns are consistent across multiple species and pervade both coding sequence and expression level variation suggests that long-term sex differences in fitness optima are significant factors influencing sex-biased gene evolution (Harrison et al 2015).…”

“…Second, there is clear evidence for adaptive divergence along the cline for well-studied traits such as cuticular hydrocarbons, which are subject to both natural and sexual selection (Higgie et al 2000;Frentiu and Chenoweth 2010). Third, precopulatory sexual selection, which may be a key form of selection influencing the evolution of sex-biased gene expression (Ellegren and Parsch 2007;Harrison et al 2015), has been directly measured along this latitudinal gradient and is known to vary in a nonclinal, population-specific manner. Finally, because D. serrata is endemic to eastern Australia, its underlying population genetic structure is less likely to represent multiple introductions and secondary contact events that can confound inferences of spatially varying selection in nonendemic species such as D.…”