Experimental evolution confirms signatures of sexual selection in genomic divergence

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 which occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequences for genomic divergence. Here we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of 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 behaviours and other sexually selected phenotypes. These are more often seen on the X chromosome, which overall shows divergence above neutral expectations. There are also characteristic signatures of selection seen in these regions, with lower diversity and greater Fst on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajima’s D implies that selective sweeps have occurred within the divergent regions, 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 in natural populations, and hence provide experimental confirmation of 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. Impact 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 straight-forward, and has been quite controversial recently. Here we used experimental evolution to allow replicate populations of fruit fly to evolve under relaxed or strengthened sexual selection for over 150 generations, then sequenced their genomes to see how they had diverged. The feature we find are very similar to those reported in populations of natural species thought to be under strong sexual selection. We found that genomic divergence was concentrated in small patches of the genome rather than widespread. These are more often seen on the X chromosome, which overall shows greatly elevated divergence. There are also characteristic signatures of selection seen in these regions, with lower genetic diversity and greater differences on the X chromosome than the autosomes. Selection was probably strong in these regions. The changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Many of the patches of divergence also contain candidate genes implicated in mating behaviours and other sexually selected phenotypes. Our results provide experimental confirmation of the likely role of sexual selection in driving such types of genetic divergence.