Negative Coupling: The Coincidence of Premating Isolating Barriers Can Reduce Reproductive Isolation

Abstract

Speciation can be mediated by a variety of reproductive barriers, and the interaction among different barriers has often been shown to enhance overall reproductive isolation, a process referred to as "coupling." Here, we analyze a population genetics model to study the establishment of linkage disequilibrium (LD) among loci involved in multiple premating barriers, an aspect that has received little theoretical attention to date. We consider a simple genetic framework underlying two distinct premating barriers, each encoded by a preference locus and its associated mating trait locus. We show that their interaction can lead to a decrease in overall reproductive isolation relative to a situation with a single barrier, a process we call "negative coupling." More specifically, in our model, negative coupling results either from sexual selection that reduces divergence at all loci, or from reduced LD that occurs because the presence of many females with "mismatched" preferences causes the mating success of recombinant males to become high. Interestingly, the latter effect may even cause LD among preference loci to become negative when recombination rates among loci are low. We conclude that coincident reproductive barriers may not necessarily reinforce each other, and that the underlying loci may not necessarily develop a positive association.