Abstract
Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography, and neutral processes that occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here, we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of allele frequency divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in “islands,” many of which contain candidate genes implicated in mating behaviors and other sexually selected phenotypes. These are more often seen on the X chromosome, which also shows greater divergence in F ST than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajima's D within some of the divergent regions may imply that selective sweeps have occurred, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex‐biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence between species and natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions.
Highlights
How does sexual selection contribute to the divergence of genomes? It is often thought that sexual selection is a potent force in evolutionary divergence, but finding “signatures” of sexual selection in the genome is not straightforward, and has been quite controversial
We found that genomic divergence was concentrated in small patches of the genome rather than widespread
Many descriptions of genomes, including those of species thought to have undergone strong sexual selection such as the Hawaiian Drosophila or African cichlids, have found that genes associated with mating behavior or sensory perception potentially involved in sexual communication are often outliers in measures of divergence (e.g., Mattersdorfer et al 2012; Kang et al 2016)
Summary
How does sexual selection contribute to the divergence of genomes? It is often thought that sexual selection is a potent force in evolutionary divergence, but finding “signatures” of sexual selection in the genome is not straightforward, and has been quite controversial. Many descriptions of genomes, including those of species thought to have undergone strong sexual selection such as the Hawaiian Drosophila or African cichlids, have found that genes associated with mating behavior or sensory perception potentially involved in sexual communication are often outliers in measures of divergence (e.g., Mattersdorfer et al 2012; Kang et al 2016) It has been known for some time that genes that diverge rapidly and show stronger signatures of positive divergent selection are often sex biased in expression (Pröschel et al 2006; Ellegren and Parsch 2007; Zhang et al 2007). Because of the femalebiased inheritance patterns of X-linked loci (males transmit them only to daughters, whereas females transmit them to both daughters and sons), sex-limited selection as well as sexual selection will influence their divergence (Mank et al 2010a; Corl and Ellegren 2012; Wright et al 2015)
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