Reduced X-linked nucleotide polymorphism inDrosophila simulans

Abstract

Population genetic theory predicts that selectively driven changes of allele frequency for both beneficial and deleterious mutants reduce polymorphism at tightly linked sites. All else being equal, these reductions in polymorphism are expected to be greater when recombination rates are lower. Therefore, the empirical observation of a positive correlation between recombination rates and amounts of DNA polymorphism across the Drosophila melanogaster genome can be explained by two very different types of natural selection. Here, we evaluate alternative models of effects of selection on linked sites by comparison of X-linked and autosomal variation. We present polymorphism data from 40 genes distributed across chromosome arms X and 3R of Drosophila simulans, a sibling species of D. melanogaster. We find significantly less silent polymorphism in D. simulans on the X chromosome than on 3R, but no difference between arms for silent divergence between species. This pattern is incompatible with predictions from theoretical studies on the effect of negative selection on linked sites. We propose that some form of positive selection having greater effects on sex chromosomes than on autosomes is the better explanation for the D. simulans data.T he amount of nucleotide polymorphism in a given region of the Drosophila melanogaster genome is positively correlated with the regional recombination rate (1, 2), which varies several-fold from one part of the genome to another (e.g., ref.3). The absence of a detectable effect of varying recombination rates on amounts of nucleotide divergence between species (1, 2) rules out variation in neutral mutation rates (4) across the genome as the explanation for the polymorphism data from D. melanogaster. Two kinds of population genetic models, both of which invoke effects of natural selection on linked neutral sites, have dominated the debate as to the cause of these patterns. One model (5-7) invokes effects of selection for beneficial mutants on linked neutral sites (i.e., hitchhiking effects), whereas a second model (8-10) invokes effects of selection against deleterious mutants on linked neutral sites (i.e., background selection). Both models predict that selection reduces polymorphism at linked neutral sites and that the magnitude of this reduction is greater when recombination rates are lower. Finally, for both models there is no expectation that variation in recombination rates affects divergence between species at neutral sites (11). The qualitatively similar predictions of the two models have made it difficult to determine their relative importance. The background selection model can provide a reasonably good fit to the polymorphism data, given certain parameters of deleterious mutation rate and recombination rate in D. melanogaster (9, 10). Similarly, a simple hitchhiking model also fits the D. melanogaster polymorphism data quite well (7, 12). Attempts to distinguish hitchhiking effects from background selection based on the frequency spectrum of variation in regions of very low cr...

Speciation through evolution of sex-linked genes

“…Masly and Presgraves (2007) suggest that disruption of dosage compensation (transcription is normally increased on the X in male Drosophila to match that in females) or of X-inactivation during spermatogenesis are more likely mechanistic explanations for the large-X effect than faster-X evolution. However, despite previous studies providing no statistical support for faster-X evolution (Begun and Whitley, 2000;Betancourt et al, 2002;Thornton et al, 2006), Begun et al (2007) recently found strong evidence for faster-X in D. simulans, D. melanogaster and D. yakuba, which they suggest may be because of higher mutation rates on the X chromosome combined with more rapid adaptive divergence. The dominance theory is strongly supported for the more slowly-evolving hybrid inviability (Coyne and Orr, 2004).…”

Chromosomal patterns of diversity and differentiation in creepers: a next-gen phylogeographic investigation of Certhia americana

“…While lower diversity has been reported in birds' sex chromosomes relative to autosomes, it is not a rule across species (Leffler et al, 2012). This pattern suggests background selection (that is, negative selection), and not directional selection, is acting on C. americana; as the Z chromosome is more efficient at removing deleterious mutations, deleterious alleles are maintained at relatively low frequencies with fewer neutral mutations linked to them (Begun and Whitley, 2000). This relationship should cause background selection to leave the Z chromosome more polymorphic, relative to autosomes, at neutral sites because fewer sites will be linked with a deleterious allele on sex chromosomes relative to autosomes.…”

“…This relationship should cause background selection to leave the Z chromosome more polymorphic, relative to autosomes, at neutral sites because fewer sites will be linked with a deleterious allele on sex chromosomes relative to autosomes. If directional selection was acting across C. americana, then the Z chromosome would be expected to have decreased diversity relative to autosomes (Begun and Whitley, 2000) because of lower effective population size and hemizygous expression in the heterogametic sex.…”

High Nucleotide Polymorphism and Rapid Decay of Linkage Disequilibrium in Wild Populations of Caenorhabditis remanei

“…Findings of comparable levels of nucleotide diversity at autosomal and X-linked loci also have been reported for several species of Drosophila (Andolfatto 2001;Dyer and Jaenike 2004), despite the potentially reduced effective population size of the X chromosome (by virtue its hemizygosity in males). Some populations of D. melanogaster and D. simulans, however, appear to have elevated (African) or reduced (non-African) levels of diversity on the X chromosome (Begun and Whitley 2000;Andolfatto 2001;Kauer et al 2002;Glinka et al 2003;Thornton and Andolfatto 2006); thus, future evaluation of diversity for C. remanei population samples from different continents might provide additional insights into the processes patterning genetic variation.…”