The Effects on Parapatric Divergence of Linkage between Preference and Trait Loci versus Pleiotropy

Attempts to uncover the genetic basis of female mating preferences and male signals involved in reproductive isolation have discovered intriguing cases in which loci contributing to these traits co-localize in their chromosomal positions. Such discoveries raise the question of whether alleles at certain loci contribute pleiotropically to male and female components of premating reproductive isolation, versus whether these loci are merely tightly linked. Here we use population genetic models to assess the degree to which these alternatives affect both short term and equilibrium patterns of trait (signal) and preference divergence. We take advantage of the fact that in the case of secondary contact between populations exchanging migrants, patterns of divergence across the range of preference strengths differ markedly when preferences and traits are controlled by the same locus (the case of phenotype matching) versus when they are on separate chromosomes. We find that tight linkage between preference and trait loci can mimic the pleiotropic pattern for many generations (roughly the reciprocal of the recombination rate), but that any recombination ultimately results in equilibrium patterns of divergence far more similar to those found when preferences and traits are on separate chromosomes. In general, our finding that pleiotropy results in quite different long-term patterns from tight linkage highlights the importance of distinguishing between these possibilities in empirical systems.