Sex-biased gene expression is repeatedly masculinized in asexual females

Darren J Parker,Jens Bast,Kirsten Jalvingh,Zoé Dumas,Marc Robinson-Rechavi,Tanja Schwander

doi:10.1038/s41467-019-12659-8

Darren J Parker, Jens Bast + Show 4 more

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https://doi.org/10.1038/s41467-019-12659-8

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Abstract

Males and females feature strikingly different phenotypes, despite sharing most of their genome. A resolution of this apparent paradox is through differential gene expression, whereby genes are expressed at different levels in each sex. This resolution, however, is likely to be incomplete, leading to conflict between males and females over the optimal expression of genes. Here we test the hypothesis that gene expression in females is constrained from evolving to its optimum level due to sexually antagonistic selection on males, by examining changes in sex-biased gene expression in five obligate asexual species of stick insect, which do not produce males. We predicted that the transcriptome of asexual females would be feminized as asexual females do not experience any sexual conflict. Contrary to our prediction we find that asexual females feature masculinized gene expression, and hypothesise that this is due to shifts in female optimal gene expression levels following the suppression of sex.

Highlights

Males and females feature strikingly different phenotypes, despite sharing most of their genome
We examine the subset of sex-biased genes that follow the expected pattern of feminisation, by looking at processes enriched for female-biased genes that increase in expression and male-biased genes that decrease in expression in asexual females
Conflict over gene expression levels between males and females is thought to drive the evolution of sex-biased gene expression[4]

Summary

Introduction

Males and females feature strikingly different phenotypes, despite sharing most of their genome. Species are able to mitigate these constraints by differentially expressing suites of genes in specific contexts to produce and maintain different phenotypes This resolution, may be incomplete when regulatory control of gene expression is not sufficiently labile as to allow for optimal expression in each phenotypic context, leading to intralocus conflict[2]. Despite the potential of this approach, previous studies have only used sexual species, examining how the transcriptome changes under experimentally altered levels of sexual selection[8,9,10,11] The premise of these studies is that because sexual selection is typically stronger on males than females[12], a reduction in sexual selection (e.g. by enforcing monogamy) will disproportionately affect males, resulting in a shift in gene expression towards the female optimum. While this optimum is unknown, it is assumed that female-biased genes are generally beneficial for females, and male-biased genes for males[4,13], such that shifts towards female optima would generate a feminisation of gene expression (increased female-biased and decreased male-biased expression)

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