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

Abstract

<jats:title>Abstract</jats:title><jats:p>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.</jats:p>

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

“…Here, our results on the evolution of disassortative mating are obtained assuming a matching rule, and we expect that assuming a preference/trait rule might limit such an evolution, because selection might break the unmatching allelic combinations. In the specific case of polymorphic mimicry, Maisonneuve et al (2019) showed that under preference/trait rule, disassortative mating can emerge only if the preference and the cue loci are fully linked.…”

“…Numerical simulations designed from the specific case of Heliconius numata, confirm that heterozygote advantage at the locus controlling color pattern variation may promote the emergence of disassortative mating (Maisonneuve et al, 2019).…”

Evolutionary insights into disassortative mating and its association to an ecologically relevant supergene

“…However the evolution of such mating behavior and its effect on polymorphism remain unclear when selection is locally positive-frequency dependent. Using a mathematical model, Maisonneuve et al [5] clarify the conditions that favor the evolution of disassortative mating in the complicated system of H. numata. In particular, they investigate whether the genetic basis of wing colour can favor the emergence of disassortative mating.…”

“…And if so, can such evolution lead to the maintenance of local polymorphism in spite of strong positive frequency-dependent selection? To investigate these questions, Maisonneuve et al [5] model evolution at two loci, one is the P locus for wing pattern, and the other influences mating behavior. The population is divided among two connected patches that differ in their butterfly communities, so that different alleles at the P locus are favored by positive frequency-dependent selection in different patches.…”

“…Such "self-referencing" mechanism of mate choice, however, has never been reported and has been argued to be rare due to its complicated nature [9]. Maisonneuve et al [5] then compare the evolution of disassortative mating via two alternative mechanisms: attraction and rejection. In these cases, alleles at the mating locus determine attraction to or rejection of specific phenotypes (e.g., under attraction rule, allele "B" encodes attraction to males with phenotype B).…”