Dispersal Alters the Nature and Scope of Sexually Antagonistic Variation

Abstract

Intra-locus sexual conflict, or sexual antagonism, occurs when alleles have opposing fitness effects in the two sexes. Previous theory suggests that sexual antagonism is a driver of genetic variation by generating balancing selection. However, these studies assume that populations are well-mixed, neglecting the effects of spatial subdivision. Here we use mathematical modelling to show that limited dispersal can fundamentally change evolution at sexually antagonistic autosomal and X-linked loci due to inbreeding and sex-specific kin competition. We find that if the sexes disperse at different rates, kin competition within the philopatric sex biases intralocus conflict in favour of the more dispersive sex. Furthermore, kin competition diminishes the strength of balancing selection relative to genetic drift, reducing genetic variation in small subdivided populations. Meanwhile, by decreasing heterozygosity, inbreeding reduces the scope for sexually antagonistic polymorphism due to non-additive allelic effects, and this occurs to a greater extent on the X-chromosome than autosomes. Overall, our results demonstrate that spatial structure is an important factor in predicting where to expect sexually antagonistic alleles. We suggest that observed interspecific and intragenomic variation in sexual antagonism may be explained by sex-specific dispersal ecology and demography.

Sexual antagonism in haplodiploids

“…This meshes with the increasing interest in the role of demography and ecology in modulating sexual antagonism (Albert and Otto 2005;Arnqvist 2011;Harts et al 2014;Tazzyman and Abbott 2015;de Vries and Caswell 2019;Hitchcock and Gardner 2020). In particular, Flintham et al (2021) have recently shown how, in viscous populations, sex-biased dispersal may skew sexual antagonism under diploidy and X-linkage toward the sex that competes less intensely with relatives. Here, we recover that same pattern, but also find that other mating schemes that characterize haplodiploid groups can involve an additional feminizing effect, as females may confer fitness benefits upon their mates.…”

“…In particular, Flintham et al. (2021) have recently shown how, in viscous populations, sex‐biased dispersal may skew sexual antagonism under diploidy and X‐linkage toward the sex that competes less intensely with relatives. Here, we recover that same pattern, but also find that other mating schemes that characterize haplodiploid groups can involve an additional feminizing effect, as females may confer fitness benefits upon their mates.…”

“…While here we focus on the additive case, it is worth noting that sib‐mating (and inbreeding more generally) will also negate the effects of dominance by inflating the proportion of individuals who are homozygous (with concomitant effects on the maintenance of polymorphisms) (Jordan and Connallon 2014; Flintham et al. 2021; SM §2.5).…”

“…We consider two variants, the first in which mating occurs before female dispersal (male dispersal $$ \to $$ mating $$ \to $$ female dispersal, DMD), and a second in which mating occurs after female dispersal (male dispersal $$ \to $$ female dispersal $$ \to $$ mating, DDM), the latter of which has been recently investigated by Flintham et al. (2021) for sexual antagonism in relation to diploidy and X‐linkage. Comparing these results, we obtain a ranking of highest potential for feminization under sib‐mating, followed by DMD, and finally DDM (Fig.…”

“…To investigate this, we contrast the above model with an alternative involving a patch structured population in which the degree of inbreeding is modulated by the extent of dispersal (Wright 1931), whereby males remain on their natal patch with probability φ m , and females with probability φ f . We consider two variants, the first in which mating occurs before female dispersal (male dispersal → mating → female dispersal, DMD), and a second in which mating occurs after female dispersal (male dispersal → female dispersal → mating, DDM), the latter of which has been recently investigated by Flintham et al (2021) for sexual antagonism in relation to diploidy and X-linkage. Comparing these results, we obtain a ranking of highest potential for feminization under sibmating, followed by DMD, and finally DDM (Fig.…”