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Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved February 24, 2015 (received for review January 26, 2015)
Significance
Genes with different expression between males and females (sex-biased genes) show rapid rates of sequence and expression divergence in a range of taxa. These characteristics have led many to assume that sex-biased genes are the product of sexual selection and sexual conflict, but this assumption remains to be rigorously tested. Using a phylogenetically controlled analysis of birds that exhibit diverse levels of sexual selection, we show a rapid turnover in sex-biased gene expression primarily through evolution of male expression levels and that the degree of sexual selection predicts the proportion of male-biased genes but does not account for rates of coding sequence evolution. We also discuss the impact of allometry on gene expression studies, an issue rarely discussed in the literature.
Abstract
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
Footnotes
- ↵1To whom correspondence should be addressed. Email: p.w.harrison{at}ucl.ac.uk.
Author contributions: P.W.H. and J.E.M. designed research; P.W.H., A.E.W., M.A.P., and J.E.M. performed research; P.W.H., A.E.W., F.Z., R.D., S.H.M., and J.E.M. contributed new reagents/analytic tools; P.W.H., A.E.W., F.Z., R.D., S.H.M., and J.E.M. analyzed data; and P.W.H., A.E.W., F.Z., R.D., S.H.M., and J.E.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequence reported in this paper has been deposited in the National Center for Biotechnology Information Short Read Archive, www.ncbi.nlm.nih.gov/sra (BioProject ID PRJNA271731).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1501339112/-/DCSupplemental.
Sexual selection and gene expression evolution
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