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 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 framwork in which to interprete empirical data on mate preferences in wild populations.

中文翻译：

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杂合子优势下一个位点杂配交配的进化和遗传结构

交配偏好的演变可能取决于对交配线索和潜在遗传结构起作用的自然选择。虽然关于局部适应性状的交配进化已经被很好地描述了，但对交配交配的进化却没有很好的描述。在这里，我们以多态拟态为例，旨在了解在强平衡选择下性状的交配交配的进化。捕食者施加的依赖于频率的正向选择会在对抗罕见变种并促进局部单态性的机翼模式上产生局部选择。这种行为跨越物种边界，有利于被保护物种的穆勒模仿。在这个特征鲜明的适应性景观中，多态模仿是罕见的，但在蝴蝶物种中观察到，与多态性染色体倒置有关。因为倒位通常与隐性有害突变相关，所以我们假设它们可能在颜色模式的基因位点诱导杂合子优势，推测有利于杂配交配的进化。为了探究无序交配出现的条件，我们对受突变负荷影响的特征位点（例如颜色模式）和偏好位点进行了建模。我们证实杂合子优势有利于解配交配的进化，并表明如果至少在性状位点的一个等位基因没有任何隐性有害突变，则更可能出现解配交配。我们对潜在的伴侣选择行为的遗传结构进行了建模，例如自我参照等位基因，或特定的偏好或排斥等位基因。我们的结果表明，与色彩模式基因座相关的自我参照或排斥等位基因可以处于正选择之下，并能够出现杂化交配。但是，仅当颜色模式和偏好位点紧密相连时，排斥等位基因才允许出现杂合交配。因此，我们的结果提供了关于选择机制和遗传结构的相关预测，有利于出现杂合交配和理论框架，其中解释了野生种群中交配偏好的经验数据。但是，仅当颜色模式和偏好位点紧密相连时，排斥等位基因才允许出现杂化交配。因此，我们的结果提供了关于选择机制和遗传结构的相关预测，有利于出现杂合交配和理论框架，其中解释了野生种群中交配偏好的经验数据。但是，仅当颜色模式和偏好位点紧密相连时，排斥等位基因才允许出现杂化交配。因此，我们的结果提供了关于选择机制和遗传结构的相关预测，有利于出现杂合交配和理论框架，其中解释了野生种群中交配偏好的经验数据。