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Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution.

Garrigan D, Kingan SB, Geneva AJ, Vedanayagam JP, Presgraves DC - Genome Biol Evol (2014)

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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Rochester dgarriga@ur.rochester.edu.

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Scans of population genetics statistics across the five major chromosomal arms of the D. mauritiana genome. The four statistics were calculated in nonoverlapping 10-kb windows. Each column of plots represents scans from a single chromosome arm. The top row of plots (blue points) shows scans of nucleotide diversity (π). The second row of plots (red points) shows the distribution of a likelihood ratio test statistic that measures the deviation of the local allele frequency spectrum (LR). The third row of plots (grey points) shows the measure of linkage disequilibrium (ZnS) across all arms. Finally, the bottom row of plots (green points) shows the scan of average sequence divergence between the ten D. mauritiana samples and a single D. melanogaster genome sequence.
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evu198-F1: Scans of population genetics statistics across the five major chromosomal arms of the D. mauritiana genome. The four statistics were calculated in nonoverlapping 10-kb windows. Each column of plots represents scans from a single chromosome arm. The top row of plots (blue points) shows scans of nucleotide diversity (π). The second row of plots (red points) shows the distribution of a likelihood ratio test statistic that measures the deviation of the local allele frequency spectrum (LR). The third row of plots (grey points) shows the measure of linkage disequilibrium (ZnS) across all arms. Finally, the bottom row of plots (green points) shows the scan of average sequence divergence between the ten D. mauritiana samples and a single D. melanogaster genome sequence.

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.—


Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution.

Garrigan D, Kingan SB, Geneva AJ, Vedanayagam JP, Presgraves DC - Genome Biol Evol (2014)

Scans of population genetics statistics across the five major chromosomal arms of the D. mauritiana genome. The four statistics were calculated in nonoverlapping 10-kb windows. Each column of plots represents scans from a single chromosome arm. The top row of plots (blue points) shows scans of nucleotide diversity (π). The second row of plots (red points) shows the distribution of a likelihood ratio test statistic that measures the deviation of the local allele frequency spectrum (LR). The third row of plots (grey points) shows the measure of linkage disequilibrium (ZnS) across all arms. Finally, the bottom row of plots (green points) shows the scan of average sequence divergence between the ten D. mauritiana samples and a single D. melanogaster genome sequence.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4202334&req=5

evu198-F1: Scans of population genetics statistics across the five major chromosomal arms of the D. mauritiana genome. The four statistics were calculated in nonoverlapping 10-kb windows. Each column of plots represents scans from a single chromosome arm. The top row of plots (blue points) shows scans of nucleotide diversity (π). The second row of plots (red points) shows the distribution of a likelihood ratio test statistic that measures the deviation of the local allele frequency spectrum (LR). The third row of plots (grey points) shows the measure of linkage disequilibrium (ZnS) across all arms. Finally, the bottom row of plots (green points) shows the scan of average sequence divergence between the ten D. mauritiana samples and a single D. melanogaster genome sequence.
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.—

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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Rochester dgarriga@ur.rochester.edu.

Show MeSH
Related in: MedlinePlus