Experimental evolution supports signatures of sexual selection in genomic divergence

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 FST 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.

Experimental sexual selection reveals rapid evolutionary divergence in sex‐specific transcriptomes and their interactions following mating

“…We found sex-and tissue-specific effects of sexual selection on gene expression and gene function, alterations in gene expression and gene function specific to origin of the female and male partners, and predicted asymmetric altered gene regulation and function arising from divergent coevolutionary trajectories between sexual selection treatments. Changes in gene expression identified here and in sex-biased gene expression in response to sexual selection(Veltsos et al, 2017) have recently been shown to be associated with genomic divergence in these lines(Wiberg et al, 2021). Overall, our results complement studies in natural populations in which sexual selection has been implicated in gene expression and genomic divergence.ACK N OWLED G EM ENTSThis work was supported by the Natural Environment Research Council (NE/I014632/1 to M.G.R., A.R.C., and R.R.S), the Natural Environment Research Council Biomolecular Analysis Facility (NBAF654 to M.G.R), and the Swedish Research Council (Vetenskapsrådet; 2018-04598 to R.R.S).…”

Domestication affects sex-biased gene expression evolution in the duck

“…This ‘illogicality’ also exists in domesticated ducks whose average Tajima's D is always more than 0.5. This genome-wide extraordinary Tajima's D results may be explained by the difference in the effective population size ( N e ) [ 55 ], which is much greater in MD than in GY and PK owing to the strong genetic bottleneck associated with domestication. This bottleneck leads to a sudden decrease of N e in domesticated ducks, and the callback effect of subsequent population expansion events was weak [ 56 ].…”

Evolutionary quantitative proteomics of reproductive interactions in Drosophila

“…Sequence and abundance divergence between species of endopeptidases and their inhibitors has been implicated in postmating prezygotic isolation across a range of taxa (16, 27, 28, 39, 80). Further analyses using divergence and polymorphism data are required to determine the evolutionary forces contributing to the fast molecular evolution of male and female derived proteins that contribute to postmating prezygotic isolation (81–84).…”