The evolution of mate choice is a major topic in evolutionary biology because it is thought to be a key factor in trait and species diversification. Here, we aim at uncovering the ecological conditions and genetic architecture enabling the puzzling evolution of disassortative mating based on adaptive traits. This rare form of mate choice is observed for some polymorphic traits but theoretical predictions on the emergence and persistence of this behavior are largely lacking. Thus, we developed a mathematical model to specifically understand the evolution of disassortative mating based on mimetic color pattern in the polymorphic butterfly Heliconius numata. 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 modeled different possible genetic architectures underlying mate choice behavior, 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 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.

AbstractThe 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.

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 evolution of disassortative preferences. We predict conditions of evolution of disassortative mating coherent with selection regimes acting on traits observed in the wild. We also show that disassortative mating generates sexual selection which disadvantages heterozygotes at the cue locus, limiting the evolution of disassortative preferences. Altogether our results partially explain why this behavior is rare in natural populations. 2