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

Abstract

Manuscript elements: Figure 1, figure 2, figure 3, table 1, online appendices A and B (including figure B1 and figure B2). Figure 1, figure 2, figure 3, figure B1 and figure B2 1 are to print in color. AbstractDisassortative mating is a rare form of mate preference that promotes the persistence 2 of polymorphism. While the evolution of assortative mating, and its consequences on trait variation and speciation have been extensively studied, the conditions enabling the 4 evolution of disassortative mating are still poorly understood. Mate preferences reduce the number of available partners, a cost that can be compensated by a greater fitness of 6 offspring. Heterozygote advantage should therefore promote the evolution of disassortative mating, which maximizes the number of heterozygous offspring. From the analysis 8 of a two-locus diploid model, with one locus controlling the mating cue under natural selection and the other locus coding for the level of disassortative preference, we show 10 that heterozygote advantage and negative frequency dependent selection acting at the cue locus promote the fixation of disassortative preferences. Interestingly, we show that 12 disassortative mating generates a negative frequency-dependent sexual selection, which in turn disadvantages heterozygotes at the cue locus, limiting the evolution of disassor-14 tative preferences. This negative feedback loop could explain why this behavior is rare in natural populations. Yet, the conditions enabling the evolution of disassortative mating 16 in our model match the selection regimes acting on traits subject to disassortative mating behavior in the wild. 18 3 34 (2006)). Moreover the mechanisms underlying mate choice may require specialized morphological, physiological and cognitive changes (see Rosenthal (2017) for a review), that 36 may induce specific metabolic costs. For example, in the self-incompatibility system in the genus Brassica, mate choice involves a specialized receptor-ligang association His-38 cock and McInnis (2003), so that the evolution of self-incompatibility is associated with metabolic costs induced by the production of the specific proteins. Mate choice can also 40 increase the investment in mate searching, because an individual needs to sample several 4 mates to find a suitable one. This increased sampling effort can be costly in time Kruijt 42