The effects of sex-biased gene expression and X-linkage on rates of adaptive protein sequence evolution in<i>Drosophila</i>

Avila, V. S. de; Campos, José Luis; Charlesworth, Brian

doi:10.1098/rsbl.2015.0117

Cited by 21 publications

(29 citation statements)

References 15 publications

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“…The difference between the X and autosomes is consistent with observations that selection on linked neutral sites has a stronger effect on the X chromosome than on the autosomes across the great apes (Hudson and Kaplan 1995; Charlesworth 1996; Orr and Betancourt 2001; Vicoso and Charlesworth 2006; Ávila et al 2015; Coolon et al 2015). Natural selection is expected to be more efficient on the X chromosome because it is hemizygous in males, and recessive alleles will be routinely exposed to selection (Vicoso and Charlesworth 2006, 2009; Coolon et al 2015).…”

Section: Discussionsupporting

confidence: 89%

Variable Autosomal and X Divergence Near and Far from Genes Affects Estimates of Male Mutation Bias in Great Apes

Narang

Sayres

2016

Genome Biol Evol

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Male mutation bias, when more mutations are passed on via the male germline than via the female germline, is observed across mammals. One common way to infer the magnitude of male mutation bias, α, is to compare levels of neutral sequence divergence between genomic regions that spend different amounts of time in the male and female germline. For great apes, including human, we show that estimates of divergence are reduced in putatively unconstrained regions near genes relative to unconstrained regions far from genes. Divergence increases with increasing distance from genes on both the X chromosome and autosomes, but increases faster on the X chromosome than autosomes. As a result, ratios of X/A divergence increase with increasing distance from genes and corresponding estimates of male mutation bias are significantly higher in intergenic regions near genes versus far from genes. Future studies in other species will need to carefully consider the effect that genomic location will have on estimates of male mutation bias.

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Section: Discussionsupporting

confidence: 89%

Variable Autosomal and X Divergence Near and Far from Genes Affects Estimates of Male Mutation Bias in Great Apes

Narang

Sayres

2016

Genome Biol Evol

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“…Ávila et al. () combined DFE‐alpha analyses of the same polymorphism and divergence data as in Campos et al. () with gene expression data from the Sebida database (Gnad & Parsch, ) to classify genes as unbiased, male‐biased or female‐biased, with genes falling below a 20% false‐positive threshold for a sex difference in expression being classified as sex‐biased.…”

Section: Empirical Findingsmentioning

confidence: 99%

Faster‐X evolution: Theory and evidence from Drosophila

2018

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A faster rate of adaptive evolution of X-linked genes compared with autosomal genes can be caused by the fixation of recessive or partially recessive advantageous mutations, due to the full expression of X-linked mutations in hemizygous males. Other processes, including recombination rate and mutation rate differences between X chromosomes and autosomes, may also cause faster evolution of X-linked genes. We review population genetics theory concerning the expected relative values of variability and rates of evolution of X-linked and autosomal DNA sequences. The theoretical predictions are compared with data from population genomic studies of several species of Drosophila. We conclude that there is evidence for adaptive faster-X evolution of several classes of functionally significant nucleotides. We also find evidence for potential differences in mutation rates between X-linked and autosomal genes, due to differences in mutational bias towards GC to AT mutations. Many aspects of the data are consistent with the male hemizygosity model, although not all possible confounding factors can be excluded.

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“…; Meisel ; Grath & Parsch ) than unbiased genes, evidence has been mixed (Meisel & Connallon ; Avila et al . , ). Furthermore, while few studies have examined sex‐specific divergence in gene expression, it also appears pronounced in male‐biased genes (Llopart ; Meisel et al .…”

Section: Introductionmentioning

confidence: 99%

Sex‐biased transcriptome divergence along a latitudinal gradient

et al. 2017

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Sex-dependent gene expression is likely an important genomic mechanism that allows sex-specific adaptation to environmental changes. Among Drosophila species, sex-biased genes display remarkably consistent evolutionary patterns; male-biased genes evolve faster than unbiased genes in both coding sequence and expression level, suggesting sex differences in selection through time. However, comparatively little is known of the evolutionary process shaping sex-biased expression within species. Latitudinal clines offer an opportunity to examine how changes in key ecological parameters also influence sex-specific selection and the evolution of sex-biased gene expression. We assayed male and female gene expression in Drosophila serrata along a latitudinal gradient in eastern Australia spanning most of its endemic distribution. Analysis of 11 631 genes across eight populations revealed strong sex differences in the frequency, mode and strength of divergence. Divergence was far stronger in males than females and while latitudinal clines were evident in both sexes, male divergence was often population specific, suggesting responses to localized selection pressures that do not covary predictably with latitude. While divergence was enriched for male-biased genes, there was no overrepresentation of X-linked genes in males. By contrast, X-linked divergence was elevated in females, especially for female-biased genes. Many genes that diverged in D. serrata have homologs also showing latitudinal divergence in Drosophila simulans and Drosophila melanogaster on other continents, likely indicating parallel adaptation in these distantly related species. Our results suggest that sex differences in selection play an important role in shaping the evolution of gene expression over macro- and micro-ecological spatial scales.

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The effects of sex-biased gene expression and X-linkage on rates of adaptive protein sequence evolution inDrosophila

Cited by 21 publications

References 15 publications

Variable Autosomal and X Divergence Near and Far from Genes Affects Estimates of Male Mutation Bias in Great Apes

Variable Autosomal and X Divergence Near and Far from Genes Affects Estimates of Male Mutation Bias in Great Apes

Faster‐X evolution: Theory and evidence from Drosophila

Sex‐biased transcriptome divergence along a latitudinal gradient

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