A gene's-eye view of sexual antagonism

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.

Sexual antagonism in haplodiploids

“…This may be important for two reasons. Firstly, sex-specific age-structure may disturb the reproductive values of males and females away from the ratios given here (Grafen 2014;Hitchcock and Gardner 2020). This may be because there are sex-differences in mortality and fecundity, such as in the citrus mealybug (Planoccocus citri) where males live up to only 3 days post eclosion whilst females can live several weeks (Nelson-Rees 1960;Ross et al 2011a), or because of other factors which can generate more cryptic age-structure such as partial bivoltinism (Seger 1983;Grafen 1986), sperm storage, or worker reproduction (Benford 1978;Charnov 1978;Alpedrinha et al 2013).…”

“…Similarly to caste structure, this may lead to trade-offs amongst these male morphs, previously termed 'intralocus tactical evolution' (Morris et al 2013). Our predictions have been derived under the assumption of non-overlapping generations, yet age-structure may also have an important modulating effect on sexual antagonism (de Vries and Caswell 2019;Hitchcock and Gardner 2020). This may be important for two reasons.…”

“…Sexual antagonism is one such example, whereby genetic variants may prove beneficial to one sex but detrimental to the other. This has motivated a large body of theoretical work considering when such sexually antagonistic alleles will be able to invade (Owen 1953), how this may vary across the genome (Parsons 1961; Kidwell et al 1977; Rice 1984; Frank and Hurst 1996; Frank and Patten 2020; Hitchcock and Gardner 2020), and how we may be able to detect such alleles from population genetic data (Cheng and Kirkpatrick 2016; Kasimatis et al 2019; Ruzicka and Connallon 2020; Ruzicka et al 2020). This theory has been complemented more recently by molecular and quantitative genetic studies of laboratory and wild populations, both estimating the extent of sexual antagonism, and identifying specific loci at which sexually antagonistic alleles reside (Poissant et al 2010; Mank 2017; Rowe et al 2018; Connallon and Matthews 2019).…”

“…Whilst similarities in transmission genetics have drawn comparisons to X-linked genes (Kraaijeveld 2009; de la Filia et al 2015), haplodiploids are not merely whole-organismal manifestations of X chromosomes. Firstly, mechanisms of dosage compensation – that ensure an equal balance of X-linked versus autosomal gene products between females and males – are understood to play an important role in modulating sexual antagonism in relation to the X chromosome (Hitchcock and Gardner 2020), but it is unclear whether these mechanisms should apply in the same way in relation to arrhenotokous species in which males are haploid across their entire genome. Secondly, although PGE is similar to X-linkage from a transmission perspective, this form of haplodiploidy involves males being somatically diploid through some or all of their lives (Burt and Trivers 2006; Gardner and Ross 2014), with concomitant gene dosage and dominance effects that may be expected to affect the balance between female-beneficial versus male-beneficial alleles.…”

“…This is conceptually similar to the X chromosomes in an XO system (or an XY system insofar as there is no homologue on the Y) and, as with X chromosomes, it is not necessarily straightforward to compare relative fitness effects across ploidy levels. If an allele’s effect is of similar magnitude in a homozygous and a hemizygous setting, then this will mean that alleles will typically have larger effects on average when expressed in males than in females (Charlesworth et al 1987; Orr and Otto 1994; Hitchcock and Gardner 2020). For example, if we consider an allele that confers a fitness effect R when in hemizygous/homozygous form, then assuming additivity and no inbreeding, a gene expressing this variant strategy will have a marginal fitness effect of ρ = R /2 when expressed in females, but ρ = R when expressed in males.…”