Ontogenetic Complexity of Sexual Dimorphism and Sex-Specific Selection

Mank, Judith E.; Nam, Kiwoong; Brunström, Björn; Ellegren, Hans

doi:10.1093/molbev/msq042

Cited by 100 publications

(135 citation statements)

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“…These results are consistent with our previous work in birds that demonstrated that sexbiased gene expression varies greatly through ontogeny and that male-and female-specific selection are ontogenetically decoupled due to sex differences in meiosis and gametogenesis (3). Although male-specific selection acts primarily on male-biased genes expressed in adults once spermatogenesis commences, female-specific selection produces a rapid rate of sequence evolution for genes that are female-biased in late development, with the onset and arrest of oogenesis before hatching (3,13). Our samples are taken from adults in their first reproductive year, as we designed the experiment to examine the power of sexual selection in shaping rates of sequence and expression evolution of male-biased genes.…”

Section: Resultsmentioning

confidence: 99%

“…Reads were mapped to these de novo assemblies to obtain sequence, expression, and polymorphism data for one-to-one orthologs between each species and the chicken genome and for one-to-one orthologs shared across the six species. Comparisons of normalized expression counts were used to identify sex-biased gene expression using standard measures and corrected for multiple testing (3,9,47). Ancestral state reconstruction was performed to predict sex bias in the most recent common ancestors from the sexbiased genes found in each of the six species.…”

Section: Methodsmentioning

confidence: 99%

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Sexual selection drives evolution and rapid turnover of male gene expression

Harrison

Wright

Zimmer

et al. 2015

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

205

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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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

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.

205

336

View full text Add to dashboard Cite

show abstract

“…Instead, it suggests that male-biased genes accumulate on sex chromosomes, even in homologous regions that still recombine between the Z and the W. In particular, whereas a lack of dosage compensation should be detectable at any developmental stage, sex-biased expression of genes (other than the sex determination genes) should be more pronounced in older embryos, after the full development of gonads (30). Consistent with more sex-specific or sexually antagonistic selection operating at later stages in development, the variance in F/M expression among autosomal genes increased from day 15-42 (P value < 2.2e−16, F test), as did the fraction of sex-biased genes (7-11% using a twofold cutoff; Tables S5-S8).…”

Section: Resultsmentioning

confidence: 99%

Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution

Vicoso

Kaiser

Bachtrog

2013

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

149

165

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Sex chromosomes originate from autosomes. The accumulation of sexually antagonistic mutations on protosex chromosomes selects for a loss of recombination and sets in motion the evolutionary processes generating heteromorphic sex chromosomes. Recombination suppression and differentiation are generally viewed as the default path of sex chromosome evolution, and the occurrence of old, homomorphic sex chromosomes, such as those of ratite birds, has remained a mystery. Here, we analyze the genome and transcriptome of emu ( Dromaius novaehollandiae ) and confirm that most genes on the sex chromosome are shared between the Z and W. Surprisingly, however, levels of gene expression are generally sex-biased for all sex-linked genes relative to autosomes, including those in the pseudoautosomal region, and the male-bias increases after gonad formation. This expression bias suggests that the emu sex chromosomes have become masculinized, even in the absence of ZW differentiation. Thus, birds may have taken different evolutionary solutions to minimize the deleterious effects imposed by sexually antagonistic mutations: some lineages eliminate recombination along the protosex chromosomes to physically restrict sexually antagonistic alleles to one sex, whereas ratites evolved sex-biased expression to confine the product of a sexually antagonistic allele to the sex it benefits. This difference in conflict resolution may explain the preservation of recombining, homomorphic sex chromosomes in other lineages and illustrates the importance of sexually antagonistic mutations driving the evolution of sex chromosomes.

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“…In evolutionary terms, these miRNAs are probably best viewed as sex-biased, as their expression pattern likely causes them to have a higher impact on fitness in one of the sexes. However, from a regulatory perspective, ovary-biased and testis-biased miRNAs may be better described as tissue-biased, since male and female gonads start diverging from a common tissue precursor in early development and have highly distinct transcriptional programs in adulthood (Mank et al 2010;Necsulea et al 2014). To study the regulatory origins of gonadal miRNA expression, a more detailed investigation of sex-biased miRNA expression throughout development would be a useful first step (Bannister et al 2009).…”

Section: Discussionmentioning

confidence: 99%

Sex-biased microRNA expression in mammals and birds reveals underlying regulatory mechanisms and a role in dosage compensation

et al. 2017

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Sexual dimorphism depends on sex-biased gene expression, but the contributions of microRNAs (miRNAs) have not been globally assessed. We therefore produced an extensive small RNA sequencing data set to analyze male and female miRNA expression profiles in mouse, opossum, and chicken. Our analyses uncovered numerous cases of somatic sex-biased miRNA expression, with the largest proportion found in the mouse heart and liver. Sex-biased expression is explained by miRNA-specific regulation, including sex-biased chromatin accessibility at promoters, rather than piggybacking of intronic miRNAs on sex-biased protein-coding genes. In mouse, but not opossum and chicken, sex bias is coordinated across tissues such that autosomal testis-biased miRNAs tend to be somatically male-biased, whereas autosomal ovary-biased miRNAs are female-biased, possibly due to broad hormonal control. In chicken, which has a Z/W sex chromosome system, expression output of genes on the Z Chromosome is expected to be male-biased, since there is no global dosage compensation mechanism that restores expression in ZW females after almost all genes on the W Chromosome decayed. Nevertheless, we found that the dominant liver miRNA, miR-122-5p, is Z-linked but expressed in an unbiased manner, due to the unusual retention of a W-linked copy. Another Z-linked miRNA, the male-biased miR-2954-3p, shows conserved preference for dosage-sensitive genes on the Z Chromosome, based on computational and experimental data from chicken and zebra finch, and acts to equalize male-to-female expression ratios of its targets. Unexpectedly, our findings thus establish miRNA regulation as a novel gene-specific dosage compensation mechanism.

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Ontogenetic Complexity of Sexual Dimorphism and Sex-Specific Selection

Cited by 100 publications

References 53 publications

Sexual selection drives evolution and rapid turnover of male gene expression

Sexual selection drives evolution and rapid turnover of male gene expression

Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution

Sex-biased microRNA expression in mammals and birds reveals underlying regulatory mechanisms and a role in dosage compensation

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