Reduced selection and accumulation of deleterious mutations in genes exclusively expressed in men

Gershoni, Moran; Pietrokovski, Shmuel

doi:10.1038/ncomms5438

Cited by 63 publications

(73 citation statements)

References 51 publications

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“…3). Such loci are under positive or purifying selection in one sex but experience the mutational input from both, which will lead to more genetic diversity than expected [49][50][51] . Consistent with this notion, recent work suggests that differences in allele frequency between males and females in humans are indeed a result of sex-specific survival 52 .…”

Section: Measuring Balancing Selection From Inter-sexual Genetic Diffmentioning

confidence: 99%

Population genetics of sexual conflict in the genomic era

2017

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ABSTRACT:Sexual conflict occurs when selection acts in opposing directions on males and females. Case studies in both vertebrates and invertebrates indicate that sexual conflict maintains genetic diversity through balancing selection, which might explain why many populations show more genetic variation than expected. Recent population genomic approaches based on different measures of balancing selection have suggested that sexual conflict can arise over survival, not just reproductive fitness as previously thought. A fuller understanding of sexual conflict will provide insight into its contribution to adaptive evolution and will reveal the constraints it might impose on populations. In many sexually reproducing species, divergent reproductive interests can arise between the sexes over courtship, fertilization and offspring investment, and these conflicting interests can lead to substantially different optimal phenotypes in males and females [1][2][3] . In such cases, selection will act in opposing directions on the sexes, a situation referred to as sexual conflict or sexual antagonism. Sexual conflict over a given phenotypic trait can occur through the interaction of alleles at two or more loci (inter-locus sexual conflict) [4][5][6] . This form of sexual conflict has been somewhat difficult to study using molecular population genetic methods, as it lacks a clear evolutionary signature in DNA sequence. As a result, the majority of recent population genomic studies have focused on cases where there are genetic trade-offs for male and female fitness from alleles at a single locus (intra-locus sexual conflict). This situation arises when male and female phenotypes are underpinned by the same genetic architecture 7 . With the exception of sex-specific Y and W chromosomes, males and females within a species share the vast majority of their genome, which creates a high potential for intra-locus conflict when male and female reproductive interests are not aligned through strict monogamy. Indeed, classic work measuring reproductive fitness in Drosophila 8 has suggested that intra-locus sexual conflict occurs at many different loci throughout the genome. Intra-locus sexual conflict can be ultimately resolved via alleles or expression patterns that are sex-specific in their effects 9-13 .The persistence of sexual conflict, and the mechanism by which it occurs, have important implications for the nature and magnitude of genetic diversity within populations [14][15][16][17][18][19] .Positive selection and purifying selection deplete populations of genetic variation over time.Nevertheless, many populations display more genetic diversity for traits under strong selection than expected, possibly because of balancing selection generated by intra-locus sexual conflict 15,20 . Intra-locus sexual conflict produces balancing selection by selecting for or against different alleles at a specific locus depending on whether they are present in females or males. The resulting genetic diversity-and by implication sexual conflictshapes t...

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Section: Measuring Balancing Selection From Inter-sexual Genetic Diffmentioning

confidence: 99%

Population genetics of sexual conflict in the genomic era

2017

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“…There are many potential causes of rapid rates of sequence evolution for sex-biased genes, including natural selection, sexual selection, and relaxed purifying selection (reduced functional pleiotropy) (Ellegren and Parsch 2007; Mank and Ellegren 2009; Parsch and Ellegren 2013), and there is considerable debate regarding whether elevated rates of evolution observed for sex-biased genes are due to adaptive (Proschel et al 2006) or nonadaptive processes (Gershoni and Pietrokovski 2014; Harrison et al 2015). Although work in Drosophila has shown that male-biased genes more often exhibit a signature of adaptive evolution (Proschel et al 2006), evidence from birds (Harrison et al 2015) and humans (Gershoni and Pietrokovski 2014) indicate relaxed constraint might be driving rapid rates of evolution.…”

Section: Introductionmentioning

confidence: 99%

Both Male-Biased and Female-Biased Genes Evolve Faster in Fish Genomes

Yang

Zhang

2016

Genome Biol Evol

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Males and females often display extensive phenotypic differences, and many of these sexual dimorphisms are thought to result from differences between males and females in expression of genes present in both sexes. Sex-biased genes have been shown to exhibit accelerated rates of evolution in a wide array of species, however the cause of this remains enigmatic. In this study, we investigate the extent and evolutionary dynamics of sex-biased gene expression in zebrafish. Our results indicate that both male-biased genes and female-biased genes exhibit accelerated evolution at the protein level. In order to differentiate between adaptive and nonadaptive causes, we tested for codon usage bias and signatures of different selective regimes in our sequence data. Our results show that both male- and female-biased genes show signatures consistent with adaptive evolution. In order to test the generality of our findings across fish, we also analyzed publicly available data on sticklebacks, and found results consistent with our findings in zebrafish.

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“…If sexual selection is driving the rapid rate of coding sequence evolution of male-biased genes, then this implies an underlying adaptive mechanism, which if true, predicts that rates of evolution for male-biased genes might be higher in species under stronger sexual selection. However, recent molecular data (16) have suggested that genes with male-limited expression have elevated levels of deleterious polymorphisms. If this is true on a broader scale, it suggests that elevated rates of evolution in male-biased genes might instead be due to relaxed purifying selection.…”

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confidence: 99%

Sexual selection drives evolution and rapid turnover of male gene expression

Harrison

Wright

Zimmer

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

193

336

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The profound and pervasive differences in gene expression observed between males and females, and the unique evolutionary properties of these genes in many species, have led to the widespread assumption that they are the product of sexual selection and sexual conflict. However, we still lack a clear understanding of the connection between sexual selection and transcriptional dimorphism, often termed sex-biased gene expression. Moreover, the relative contribution of sexual selection vs. drift in shaping broad patterns of expression, divergence, and polymorphism remains unknown. To assess the role of sexual selection in shaping these patterns, we assembled transcriptomes from an avian clade representing the full range of sexual dimorphism and sexual selection. We use these species to test the links between sexual selection and sex-biased gene expression evolution in a comparative framework. Through ancestral reconstruction of sex bias, we demonstrate a rapid turnover of sex bias across this clade driven by sexual selection and show it to be primarily the result of expression changes in males. We use phylogenetically controlled comparative methods to demonstrate that phenotypic measures of sexual selection predict the proportion of male-biased but not female-biased gene expression. Although male-biased genes show elevated rates of coding sequence evolution, consistent with previous reports in a range of taxa, there is no association between sexual selection and rates of coding sequence evolution, suggesting that expression changes may be more important than coding sequence in sexual selection. Taken together, our results highlight the power of sexual selection to act on gene expression differences and shape genome evolution.sperm competition | sex-biased gene expression | gene expression evolution | sexual dimorphism | sexual conflict N umerous studies across a range of organisms have convergently shown that the majority of variation in overall gene expression is explained by sex (1-6). These sex-biased genes have distinct evolutionary properties, namely they show faster rates of sequence and expression divergence, as well as rapid rates of turnover, broadly consistent with sexual selection (7, 8). The sizable proportion of genes exhibiting sex-biased expression suggests that sexual selection has the potential to shape many aspects of genome biology. Recent studies of intrasexual variation in gene expression differences between males and females of the same species have revealed patterns of overall transcription consistent with the degree of phenotypic sexual dimorphism (9, 10), and experimental manipulation of sex-specific selection affects sex-biased gene expression over short time scales (11-13). These studies together suggest that increasing sexual selection across species should lead to increased turnover in sex-biased gene expression and a greater sexualization of the transcriptome over longer evolutionary timescales.The elevated rates of coding sequence evolution often (14) but not always (15) observed for m...

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Reduced selection and accumulation of deleterious mutations in genes exclusively expressed in men

Cited by 63 publications

References 51 publications

Population genetics of sexual conflict in the genomic era

Population genetics of sexual conflict in the genomic era

Both Male-Biased and Female-Biased Genes Evolve Faster in Fish Genomes

Sexual selection drives evolution and rapid turnover of male gene expression

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