A supergene in seaweed flies modulates male traits and female perception

Supergenes, tightly linked allelic combinations that underlie complex adaptive phenotypes represent a critical mechanism protecting intra-specific polymorphism. Supergenes represent some of the best examples of balancing selection in nature and there is increasing evidence that disassortative mating, when individuals preferentially mate with dissimilar phenotypes, is a key force stabilizing supergene polymorphisms. Yet, the underlying biological mechanisms and genetic basis of disassortative mating remain poorly known. Here, we examine a possible mechanism of disassortative mating driven by female mate choice in relation to the overdominant Cf-Inv(1) supergene in the seaweed fly Coelopa frigida by investigating chemical communication and its genomic architecture. We show that Cf-Inv(1) strongly affects chemical signaling; cuticular hydrocarbon (CHC) composition differed between genotypes in males but not females across two continents. In tandem, Cf-Inv(1) affected female perception of these compounds; females are able to sense 36 compounds from the male CHC cocktail but show differential perception between genotypes for almost half of them. This indicates that the genetic underpinnings of male traits and female perceptions are tightly linked within Cf-Inv(1) which likely facilitates disassortative mating. A differential expression approach based on candidate genes for CHC biosynthesis and odorant detection revealed differential expression for CHC biosynthesis in males alone but broad changes in odorant receptors across both sexes. Furthermore, odorant genes clustered together within Cf-Inv(1), with some of them differing between arrangements by 8.3% at the protein level, suggesting evolution via tandem duplication then divergence. We propose that the tight linkage between overdominant loci, male traits, and female perception has helped to maintain the Cf-Inv(1) polymorphism across its range in the face of supergene degeneration.

An investigation of MHC-dependent sexual selection in a free-living population of sheep

MHC genes are one of the most polymorphic gene clusters in vertebrates and play an essential role in adaptive immunity. There is evidence that sexual selection also plays a role in maintaining MHC diversity, but the specific mechanisms are controversial. In this study, we investigate evidence for non-random MHC-dependent mating patterns in a free-living population of Soay sheep. Using a large number of sheep diplotyped at the MHC class IIa region and genome-wide SNPs, together with field observations of consorts, we found sexual selection against one of eight haplotypes, C, in males at the pre-copulatory stage and sexual selection on female MHC heterozygosity acting in opposition directions at the pre- and post-copulatory stages. We also found disassortative mating at the post-copulatory stage, along with strong evidence of inbreeding avoidance at both stages. However, results from generalized linear mixed models suggest that the pattern of MHC-dependent disassortative mating could be a by-product of inbreeding avoidance. These results suggest that there is selection on the MHC at the pre- and post-copulatory stages, but that apparent disassortative mating with respect to the MHC may be driven by inbreeding avoidance.

When do opposites attract? A model uncovering the evolution of disassortative mating

Disassortative mating is a rare form of mate preference that promotes the persistence of polymorphism. While the evolution of assortative mating, and its consequences on trait variation and speciation have been extensively studied, the conditions enabling the evolution of disassortative mating are still poorly understood. Mate preferences increase the risk of missing mating opportunities, a cost that can be compensated by a greater fitness of offspring. Heterozygote advantage should therefore promote the evolution of disassortative mating, which maximizes the number of heterozygous offspring. From the analysis of a two-locus diploid model, with one locus controlling the mating cue under viability selection and the other locus coding for the level of disassortative preference, we show that heterozygote advantage and negative frequency-dependent viability selection acting at the cue locus promote the fixation of disassortative preferences. The conditions predicted to enable the evolution of disassortative mating in our model match the selection regimes acting on traits subject to disassortative mating behavior in the wild. In sharp contrast with the evolution of assortative preferences, we also show that disassortative mating generates a negative frequency-dependent sexual selection, which in turn disadvantages heterozygotes at the cue locus, limiting the evolution of disassortative preferences. This negative feedback loop could explain why this behavior is rare in natural populations.

Distribution of facial resemblance in romantic couples suggests both positive and negative assortative processes influence human mate choice

Previous research suggests that humans show positive assortative mating, i.e. tend to pair up with partners that are similar to themselves in a range of traits, including facial appearance. Facial appearance can function as a cue to genetic similarity and plays a critical role in human mate choice. Evidence for positive assortative mating for facial appearance has largely come from studies showing people can match pictures of couples’ faces at levels greater than chance and that facial photographs of couples are rated to look more similar than those of non-couples. However, interpreting results from matching studies as evidence of positive assortative mating for facial appearance is problematic, since this measure of perceived compatibility does not necessarily reflect actual physical similarity, and may be orthogonal to, or even negatively correlated with, physical similarity. Even if participants are asked to rate facial similarity directly, it remains unclear which, if any, face shape cues contribute to an increased perception of similarity in romantic couples. Here we use a shape-based assessment of facial similarity to show that the median similarity of long-term couples’ face shapes is only slightly greater than that of an age-matched control sample. Moreover, this was driven by the most similar 40% of couples, while the most dissimilar 20% of couples actually showed disassortative mating for face shape when compared to the control sample. These data show that a simple measure of central tendency obscures variability in the extent to which couples display assortative or disassortative mating for face shape. By contrast, a more fine-grained analysis that considers the distribution of variation across couples in the extent to which they resemble each other suggests that both positive and negative assortative processes influence human mate choice.

No evidence of positive assortative mating for genetic quality in fruit flies

In sexual populations, the effectiveness of selection will depend on how gametes combine with respect to genetic quality. If gametes with deleterious alleles are likely to combine with one another, deleterious genetic variation can be more easily purged by selection. Assortative mating, where there is a positive correlation between parents in a phenotype of interest such as body size, is often observed in nature, but does not necessarily reveal how gametes ultimately combine with respect to genetic quality itself. We manipulated genetic quality in fruit fly populations using an inbreeding scheme designed to provide an unbiased measure of mating patterns. While inbred flies had substantially reduced reproductive success, their gametes did not combine with those of other inbred flies more often than expected by chance, indicating a lack of positive assortative mating. Instead, we detected a negative correlation in genetic quality between parents, i.e. disassortative mating, which diminished with age. This pattern is expected to reduce the genetic variance for fitness, diminishing the effectiveness of selection. We discuss how mechanisms of sexual selection could produce a pattern of disassortative mating. Our study highlights that sexual selection has the potential to either increase or decrease genetic load.

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

The evolution of mate preferences may depend on natural selection acting on the mating cues and on the underlying genetic architecture. While the evolution of assortative mating with respect to locally adapted traits has been well-characterized, the evolution of disassortative mating is poorly characterized. Here we aim at understanding the evolution of disassortative mating for traits under strong balancing selection, by focusing on polymorphic mimicry as an illustrative example. Positive frequency-dependent selection exerted by predators generates local selection on wing patterns acting against rare variants and promoting local monomorphism. This acts across species boundaries, favouring Mullerian mimicry among defended species. In this well-characterized adaptive landscape, polymorphic mimicry is rare but is observed in a butterfly species, associated with polymorphic chromosomal inversions. Because inversions are often associated with recessive deleterious mutations, we hypothesize they may induce heterozygote advantage at the color pattern locus, putatively favoring the evolution of disassortative mating. To explore the conditions underlying the emergence of disassortative mating, we modeled both a trait locus (colour pattern for instance), subject to mutational load, and a preference locus. We confirm that heterozygote advantage favors the evolution of disassortative mating and show that disassortative mating is more likely to emerge if at least one allele at the trait locus is free from any recessive deleterious mutations. We modelled different possible genetic architectures underlying mate choice behaviour, such as self referencing alleles, or specific preference or rejection alleles. Our results showed that self referencing or rejection alleles linked to the color pattern locus can be under positive selection and enable the emergence of disassortative mating. However rejection alleles allow the emergence of disassortative mating only when the color pattern and preference loci are tightly linked. Our results therefore provide relevant predictions on both the selection regimes and the genetic architecture favoring the emergence of disassortative mating and a theoretical framework in which to interprete empirical data on mate preferences in wild populations.

Genomic evidence for MHC disassortative mating in humans

Although pervasive in many animal species, the evidence for major histocompatibility complex (MHC) disassortative mating in humans remains inconsistent across studies. Here, to revisit this issue, we analyse dense genotype data for 883 European and Middle Eastern couples. To distinguish MHC-specific effects from socio-cultural confounders, the pattern of relatedness between spouses in the MHC region is compared to the rest of the genome. Couples from Israel exhibit no significant pattern of relatedness across the MHC region, whereas across the genome, they are more similar than random pairs of individuals, which may reflect social homogamy and/or cousin marriages. On the other hand, couples from The Netherlands and more generally from Northern Europe are significantly more MHC-dissimilar than random pairs of individuals, and this pattern of dissimilarity is extreme when compared with the rest of the genome. Our findings support the hypothesis that the MHC influences mate choice in humans in a context-dependent way: MHC-driven preferences may exist in all populations but, in some populations, social constraints over mate choice may reduce the ability of individuals to rely on such biological cues when choosing their mates.