Abstract:Sex‐specific dominance reversals (SSDRs) in fitness‐related traits, where heterozygotes' phenotypes resemble those of alternative homozygotes in females versus males, can simultaneously maintain genetic variation in fitness and resolve sexual conflict and thereby shape key evolutionary outcomes. However, the full implications of SSDRs will depend on how they arise and the resulting potential for evolutionary, ecological and environmental modulation. Recent field and laboratory studies have demonstrated SSDRs i… Show more
“…Because such dominance relationships may result from fitness landscapes declining slowly away from phenotypic optima (i.e. showing diminishing returns to adaptation [37], as found on Gaussian fitness landscapes), multiple authors have suggested that favourable conditions for sexually antagonistic polymorphism may be common, especially in well-adapted populations [5,10,14,15,30,[38][39][40][41][42][43] (where landscapes typically show diminishing returns [44,45]).…”
Section: Introductionmentioning
confidence: 99%
“…One salient point from this theory is that sexual antagonism can maintain a balanced genetic polymorphism for two alleles at a locus either when selection is strong and symmetrical between the sexes, or when allelic dominance is sex-specific such that alleles are more dominant when beneficial and more recessive when deleterious ("sex-specific dominance reversal" [18,23,30]). Because such dominance relationships can result from fitness landscapes declining slowly away from phenotypic optima (i.e., showing diminishing returns to adaptation [37,38]), it has been suggested that sexually antagonistic balancing selection may be common, especially in well-adapted populations [5,10,23,30,[38][39][40][41][42][43][44]. Furthermore, even when sexually antagonistic polymorphism is not balanced and therefore ephemeral, it may nevertheless persist for longer than other non-neutral variation due to opposing selection in males and females [26,27].…”
Selection often favours different trait values in males and females, leading to genetic conflicts between the sexes, or sexual antagonism. Theory suggests that such conflict can maintain genetic variation by generating balancing selection. However, most of this theory is based on insights from models of single loci with fixed fitness effects. It is thus unclear how readily sexual antagonism drives balancing selection at loci where the fitness effects are not arbitrarily set but emerge from the genotype-phenotype map and the fitness landscape. Here we use mathematical models and computer simulations to investigate the evolution of traits that have different optima in males and females and so experience sexually antagonistic selection. We examine the consequences of such selection for the maintenance and nature of genetic variation under different assumptions of genetic architecture and for different fitness landscapes. We show that the conditions necessary to maintain variation are significantly more restrictive than previously appreciated. This is because the majority of typical sex-specific fitness landscapes generate stabilising selection on traits, and so favour the fixation of a single homozygote genotype that encodes the phenotype with the highest sex-averaged fitness. Instead, the maintenance of genetic polymorphism requires extremely, if not implausibly, strong conflict between males and females in order to disfavour extreme and intermediate phenotypes by generating diversifying selection. Furthermore, in all cases, we find that distinctive patterns of genetic variation produced by sexual antagonism arise rarely and are often transient, and so are difficult to observe in genomic data. Taken together, our results indicate that sex-specific selection is not a straightforward source of balanced genetic polymorphism and leaves few traces in the genome. Rather, we suggest that sexual antagonism is most likely to maintain genetic variation when traits are determined by a single large effect locus where genetic constraints lead to a limited range of possible alleles.
“…Because such dominance relationships may result from fitness landscapes declining slowly away from phenotypic optima (i.e. showing diminishing returns to adaptation [37], as found on Gaussian fitness landscapes), multiple authors have suggested that favourable conditions for sexually antagonistic polymorphism may be common, especially in well-adapted populations [5,10,14,15,30,[38][39][40][41][42][43] (where landscapes typically show diminishing returns [44,45]).…”
Section: Introductionmentioning
confidence: 99%
“…One salient point from this theory is that sexual antagonism can maintain a balanced genetic polymorphism for two alleles at a locus either when selection is strong and symmetrical between the sexes, or when allelic dominance is sex-specific such that alleles are more dominant when beneficial and more recessive when deleterious ("sex-specific dominance reversal" [18,23,30]). Because such dominance relationships can result from fitness landscapes declining slowly away from phenotypic optima (i.e., showing diminishing returns to adaptation [37,38]), it has been suggested that sexually antagonistic balancing selection may be common, especially in well-adapted populations [5,10,23,30,[38][39][40][41][42][43][44]. Furthermore, even when sexually antagonistic polymorphism is not balanced and therefore ephemeral, it may nevertheless persist for longer than other non-neutral variation due to opposing selection in males and females [26,27].…”
Selection often favours different trait values in males and females, leading to genetic conflicts between the sexes, or sexual antagonism. Theory suggests that such conflict can maintain genetic variation by generating balancing selection. However, most of this theory is based on insights from models of single loci with fixed fitness effects. It is thus unclear how readily sexual antagonism drives balancing selection at loci where the fitness effects are not arbitrarily set but emerge from the genotype-phenotype map and the fitness landscape. Here we use mathematical models and computer simulations to investigate the evolution of traits that have different optima in males and females and so experience sexually antagonistic selection. We examine the consequences of such selection for the maintenance and nature of genetic variation under different assumptions of genetic architecture and for different fitness landscapes. We show that the conditions necessary to maintain variation are significantly more restrictive than previously appreciated. This is because the majority of typical sex-specific fitness landscapes generate stabilising selection on traits, and so favour the fixation of a single homozygote genotype that encodes the phenotype with the highest sex-averaged fitness. Instead, the maintenance of genetic polymorphism requires extremely, if not implausibly, strong conflict between males and females in order to disfavour extreme and intermediate phenotypes by generating diversifying selection. Furthermore, in all cases, we find that distinctive patterns of genetic variation produced by sexual antagonism arise rarely and are often transient, and so are difficult to observe in genomic data. Taken together, our results indicate that sex-specific selection is not a straightforward source of balanced genetic polymorphism and leaves few traces in the genome. Rather, we suggest that sexual antagonism is most likely to maintain genetic variation when traits are determined by a single large effect locus where genetic constraints lead to a limited range of possible alleles.
“…The degree to which the evolution of dominance is constrained has been a matter of some debate (Otto and Bourguet, 1999;Grieshop et al, 2024), but it is clear that sex-specific dominance for phenotypic traits could emerge either through nonlinearities in the manner in which allelic effects are translated into phenotypes (Wright, 1934;Kacser and Burns, 1981;Otto and Bourguet, 1999;Reid, 2022) or through dominance modifiers (Spencer and Priest, 2016;Grieshop et al, 2024). Second, unlike previous theory studying the implications of sex-specific dominance, our model is not restricted to BAP.…”
Section: Discussionmentioning
confidence: 99%
“…The fact that we observe sex-specific dominance emerging in our model is, although consequential, perhaps not surprising: the evolution of adaptive dominance is predicted when polymorphism is maintained by marginal overdominance, as this increases heterozygote fitness (Fisher, 1931). The degree to which the evolution of dominance is constrained has been a matter of some debate (Otto and Bourguet, 1999; Grieshop et al, 2024), but it is clear that sex-specific dominance for phenotypic traits could emerge either through nonlinearities in the manner in which allelic effects are translated into phenotypes (Wright, 1934; Kacser and Burns, 1981; Otto and Bourguet, 1999; Reid, 2022) or through dominance modifiers (Spencer and Priest, 2016; Grieshop et al, 2024).…”
Sexually antagonistic (SA) selection, favouring different alleles in males and females, can contribute to the maintenance of genetic diversity. While current theory predicts that biallelic polymorphism can be maintained in SA loci, particularly with strong selection or sex-specific dominance, some candidate SA loci harbour more than two segregating alleles. This highlights a gap in our understanding of the origin and maintenance of SA genetic variation. We present a mathematical model to explore the evolution of alleles at either an autosomal or an X-linked locus under SA selection, affecting a quantitative trait with distinct female and male optima. We show that additive allelic effects predict only biallelic polymorphism, and only under symmetric and relatively strong selection. Polyallelic polymorphism can evolve under conditions of sex-specific or X-linked dominance for the trait, particularly under weak selection, such that several alleles coexist in a single population through balancing selection. Our analysis furthermore shows that sex-specific dominance (and X-linked dominance) evolves when permitted, thus promoting the evolution of polyallelic polymorphism. We conclude that SA selection can drive the co-evolution of sex-specific dominance and polyallelic polymorphism, particularly under weak selection, which reduces the gender load. To assess these findings, we analyse segregating variation in three populations of a seed beetle model system and find support for our predictions: (i) candidate SA loci show a relatively strong signal of polyallelic polymorphism and (ii) loci with the strongest signal of polyallelic polymorphism are enriched with genes associated with known SA phenotypes.
“…Note, however, that trait-level dominance reversals may or may not be dominance reversed for fitness, per se , depending on how the phenotype maps to fitness. In principle, dominance reversals at the phenotypic level could occur due to traits being threshold-like (non-linear genotype–phenotype relationship) [ 103 ], or could arise due to the explicit action of a dominance modifier [ 62 ]. Figure 1 Graphical representation of beneficial dominance reversals.…”
Section: Evolutionary Causes Of Dominance Reversalsmentioning
Beneficial reversals of dominance reduce the costs of genetic trade-offs and can enable selection to maintain genetic variation for fitness. Beneficial dominance reversals are characterized by the beneficial allele for a given context (e.g. habitat, developmental stage, trait or sex) being dominant in that context but recessive where deleterious. This context dependence at least partially mitigates the fitness consequence of heterozygotes carrying one non-beneficial allele for their context and can result in balancing selection that maintains alternative alleles. Dominance reversals are theoretically plausible and are supported by mounting empirical evidence. Here, we highlight the importance of beneficial dominance reversals as a mechanism for the mitigation of genetic conflict and review the theory and empirical evidence for them. We identify some areas in need of further research and development and outline three methods that could facilitate the identification of antagonistic genetic variation (dominance ordination, allele-specific expression and allele-specific ATAC-Seq (assay for transposase-accessible chromatin with sequencing)). There is ample scope for the development of new empirical methods as well as reanalysis of existing data through the lens of dominance reversals. A greater focus on this topic will expand our understanding of the mechanisms that resolve genetic conflict and whether they maintain genetic variation.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
