Maintenance of Variation between Linked Loci under Ecological and Sexual Selection

Reproductive barriers are a key contribution to speciation; female preference for a male mating signal is a prezygotic barrier both empirically documented and theoretically studied. Genes that encode components of a reproductive barrier are more likely to retain variation when they occur simultaneously with genes under direct environmental selection. Theoreticians often make the assumption of a single gene controlling both effects or a “magic” trait, which have been identified in several empirical cases. The effects of a magic trait can be replicated by two colocalized genes: one under environmental selection, and one that encodes a mate signal or preference independently; this case is referred to as a pseudomagic trait complex. It is not known, however, what conditions lead to the genomic colocalization of genes underlying different effects to form such a pseudomagic trait. This study investigates the colocalization of mate signal loci and loci under ecological selection, to determine whether the rate of recombination between these is important in determining whether variation will be maintained at mate signal loci. An individual-based genomic model was used to provide finer detail on the genomic conditions that lead to divergence in signal across two demographic groups. To model variation in recombination rates, loci from each effect were clustered into two generally overlapping regions. It was confirmed that tight physical linkage between ecological and signal loci led to maintained signal phenotypic variation: divergence among many small-effect signal loci were only maintained when genomic regions were close and compact, and the loci that retain divergence were often characterized by tight linkage with ecological loci. This suggests that loose recombination between the components of a pseudomagic trait facilitates even tighter recombination so that a pseudomagic trait complex is formed.