Population genetics of sexual conflict in the genomic era

Abstract

ABSTRACT:Sexual conflict occurs when selection acts in opposing directions on males and females. Case studies in both vertebrates and invertebrates indicate that sexual conflict maintains genetic diversity through balancing selection, which might explain why many populations show more genetic variation than expected. Recent population genomic approaches based on different measures of balancing selection have suggested that sexual conflict can arise over survival, not just reproductive fitness as previously thought. A fuller understanding of sexual conflict will provide insight into its contribution to adaptive evolution and will reveal the constraints it might impose on populations. In many sexually reproducing species, divergent reproductive interests can arise between the sexes over courtship, fertilization and offspring investment, and these conflicting interests can lead to substantially different optimal phenotypes in males and females [1][2][3] . In such cases, selection will act in opposing directions on the sexes, a situation referred to as sexual conflict or sexual antagonism. Sexual conflict over a given phenotypic trait can occur through the interaction of alleles at two or more loci (inter-locus sexual conflict) [4][5][6] . This form of sexual conflict has been somewhat difficult to study using molecular population genetic methods, as it lacks a clear evolutionary signature in DNA sequence. As a result, the majority of recent population genomic studies have focused on cases where there are genetic trade-offs for male and female fitness from alleles at a single locus (intra-locus sexual conflict). This situation arises when male and female phenotypes are underpinned by the same genetic architecture 7 . With the exception of sex-specific Y and W chromosomes, males and females within a species share the vast majority of their genome, which creates a high potential for intra-locus conflict when male and female reproductive interests are not aligned through strict monogamy. Indeed, classic work measuring reproductive fitness in Drosophila 8 has suggested that intra-locus sexual conflict occurs at many different loci throughout the genome. Intra-locus sexual conflict can be ultimately resolved via alleles or expression patterns that are sex-specific in their effects 9-13 .The persistence of sexual conflict, and the mechanism by which it occurs, have important implications for the nature and magnitude of genetic diversity within populations [14][15][16][17][18][19] .Positive selection and purifying selection deplete populations of genetic variation over time.Nevertheless, many populations display more genetic diversity for traits under strong selection than expected, possibly because of balancing selection generated by intra-locus sexual conflict 15,20 . Intra-locus sexual conflict produces balancing selection by selecting for or against different alleles at a specific locus depending on whether they are present in females or males. The resulting genetic diversity-and by implication sexual conflictshapes t...

A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

“…One hypothesis for this observation is that by chance Chromosome 2 carries an excess of loci with sex‐biased expression. This situation could result if there are many loci on that chromosome that experience SAS, which can lead to the evolution of sex‐biased expression (Cheng & Kirkpatrick, ; Grath & Parsch, ; Mank, ; Parsch & Ellegren, ). SAS acting on Chromosome 2 could also be the driving force for the fixation of the reciprocal translocation in Ammarnäs (discussed below).…”

Sexual conflict and the maintenance of genetic variation in natural populations

“…If the selection pressures act in opposite directions in males and females, we refer to this as (inter‐) sexual conflict or sexual antagonism (Arnqvist & Rowe, ). Testing if sexual conflict maintains genetic variation in natural populations is a tremendous challenge—it requires both identifying loci that harbor sexually antagonistic alleles and determining whether those alleles are maintained as stable polymorphisms (Mank, ). Doing so genome‐wide is even harder because it is not tractable to identify sexually antagonistic alleles and test for stable polymorphisms at all loci.…”

“…It has therefore been predicted that sexual conflict can maintain genetic variation in a manner similar to other forms of balancing selection (Kidwell et al., ; Owen, ). Indeed, a few large‐effect sexually antagonistic alleles have been identified that appear to be maintained as balanced polymorphisms (Mank, ).…”

“…Despite the evidence from a few case studies, previous work has not tested the extent to which sexual conflict maintains allelic variation genome‐wide (Mank, ). Dutoit et al.…”

“…This interpretation is consistent with an experiment that found very few Drosophila genes with sex‐biased expression that are associated with ongoing sexually antagonistic fitness effects (Innocenti & Morrow, ). Despite the weak empirical links between gene expression and ongoing sexual conflict, genes with sex‐biased expression are typically inferred to harbor sexually antagonistic alleles at some point in time—either in the past, in the present or both (Mank, ).…”