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 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.

Selection on the fly: short term adaptation to an altered sexual selection regime inDrosophila pseudoobscura

“…5 ). These results are consistent with the findings by Wiberg et al (2021) whose SNPs showing significantly consistent allele frequency differences between E and M clustered along chromosomes 3 and X. The selection signatures we find are more pervasive in comparison to Wiberg et al’s “islands” of differentiation.…”

“…6). Wiberg et al (2021) previously identified 480 variants as having a significant allele frequency differences between M and E replicates at time point 3. We determined which genes these top SNPs were located in as well as any genes in the vicinity of intergenic top SNPs.…”

“…Samples at time point 4 were sequenced as part of Wiberg et al (2021). DNA sequencing was carried out at Novogene (Hong Kong) using an Illumina HiSeq X Ten platform.…”

Experimental sexual selection affects the evolution of physiological and life history traits

“…Additionally, coevolutionary patterns have been found, such that E males are more harmful but E females more resilient to such harm [36,37], and females prefer courtship song of males from their own treatment [33]. These evolved phenotypic differences are accompanied by divergence in gene expression [38,39] and concerted genetic differences between treatments [40]. In the present study, we tested whether the mating system similarly caused life history and metabolic traits to evolve, which we tested by measuring respiration, macro-metabolites, and developmental traits.…”

“…Additionally, coevolutionary patterns have been found, such that E males are more harmful but E females more resilient to such harm (Crudgington et al, 2005(Crudgington et al, , 2009, and females prefer courtship song of males from their own treatment (Debelle et al, 2014). These evolved phenotypic differences are accompanied by divergence in gene expression (Immonen et al, 2014;Veltsos et al, 2017) and concerted genetic differences between treatments (Wiberg et al, 2021). Given these evolved differences in traits directly associated with reproduction, we tested whether the mating system similarly caused divergence in life history and physiological phenotypes that likely contribute to reproductive success, namely metabolic rate, macrometabolite content, development time, and stress resistance.…”