A gene's-eye view of sexual antagonism.

Thomas J Hitchcock,Andy Gardner

doi:10.1098/rspb.2020.1633

Thomas J Hitchcock, Andy Gardner

Open Access

https://doi.org/10.1098/rspb.2020.1633

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Abstract

Females and males may face different selection pressures. Accordingly, alleles that confer a benefit for one sex often incur a cost for the other. Classic evolutionary theory holds that the X chromosome, whose sex-biased transmission sees it spending more time in females, should value females more than males, whereas autosomes, whose transmission is unbiased, should value both sexes equally. However, recent mathematical and empirical studies indicate that male-beneficial alleles may be more favoured by the X chromosome than by autosomes. Here we develop a gene's-eye-view approach that reconciles the classic view with these recent discordant results, by separating a gene's valuation of female versus male fitness from its ability to induce fitness effects in either sex. We use this framework to generate new comparative predictions for sexually antagonistic evolution in relation to dosage compensation, sex-specific mortality and assortative mating, revealing how molecular mechanisms, ecology and demography drive variation in masculinization versus feminization across the genome.

Highlights

New genomic approaches paint an increasingly vivid picture of the extent of sexual antagonism across the genome, identifying specific loci at which fixed or segregating alleles increase the fitness of their female carriers while decreasing the fitness of their male carriers, or vice versa [1,2]
The overall action of natural selection on such alleles depends on how the benefits enjoyed by one sex are balanced by costs incurred by the other, and since different parts of the genome are expected to place different values on the fitness of females and males this is predicted to lead to an intragenomic conflict of interest with respect to sexually antagonistic traits [3,4,5,6,7,8]
The X chromosome has been viewed as placing twice as much value on the fitness of females as it does the fitness of males, on account of it spending twice as much evolutionary time in the bodies of females than in the bodies of males, whereas the autosomes have been viewed as placing equal value on each sex on account of them spending an equal portion of evolutionary time being carried by males and females [9,10,11,12,13,14,15,16]

Summary

Introduction

New genomic approaches paint an increasingly vivid picture of the extent of sexual antagonism across the genome, identifying specific loci at which fixed or segregating alleles increase the fitness of their female carriers while decreasing the fitness of their male carriers, or vice versa [1,2]. If autosomal genes place equal value on the fitness of females and males, the condition for invasion of a mutant allele is σ > τ, which is equivalent to S > T, in agreement with the above analysis.

Results

Conclusion