Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution.
Bottom Line: Our analyses show that, relative to the autosomes, the X chromosome has reduced nucleotide diversity but elevated nucleotide divergence; an excess of recurrent adaptive evolution at its protein-coding genes; an excess of recent, strong selective sweeps; and a large excess of satellite DNA.Furthermore, genes with roles in reproduction and chromosome biology are enriched among genes that have histories of recurrent adaptive protein evolution.Together, these genome-wide analyses suggest that genetic conflict and frequent positive natural selection on the X chromosome have shaped the molecular evolutionary history of D. mauritiana, refining our understanding of the possible causes of the large X-effect in speciation.
Affiliation: Department of Biology, University of Rochester firstname.lastname@example.org.Show MeSH
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Mentions: We surveyed nucleotide polymorphism and divergence from D. melanogaster in 10-kb windows for ten D. mauritiana genomes (fig. 1). Compared with the autosomes, the X chromosome has significantly elevated divergence (dX/dA = 1.100), but reduced polymorphism (πX/πA = 0.649; table 1, Mann–Whitney U tests, PMWU < 2.2 × 10−16). These contrasting X/A ratios for polymorphism and divergence cannot be explained by a standard neutral model, assuming no selection, an equal breeding sex ratio, and constant effective population size (Ne), such that Ne,X/Ne,A = ¾. Furthermore, the observed πX/πA ratio of nucleotide diversity is difficult to reconcile with an extreme founder event (Pool and Nielsen 2008), for which there is no evidence in the recent history of D. mauritiana. The X/A ratios of polymorphism and divergence are however consistent with a model involving selection. First, under a model of nearly neutral evolution, slightly deleterious substitutions can accumulate faster on the X than on the autosomes. Assuming new mutations have scaled selection coefficients of Nes −3 (or weaker), and assuming Ne,X/Ne,A 0.65 (as observed), then the X chromosome is expected to experience a higher rate of substitution than the autosomes, regardless of dominance (Vicoso and Charlesworth 2009). Second, under a model of adaptive evolution, beneficial mutations can accumulate on the X more quickly than on the autosomes (Charlesworth et al. 1987; Vicoso and Charlesworth 2009). Assuming new beneficial mutations tend to be recessive, then the X/A ratios of polymorphism and divergence could be consistent with a model of recurrent hitchhiking in which selective sweeps on the X chromosome are more frequent, stronger, and/or more often involve new beneficial mutations rather than standing genetic variation (Begun and Whitley 2000; Orr and Betancourt 2001; Betancourt et al. 2004).Fig. 1.—
Affiliation: Department of Biology, University of Rochester email@example.com.