Extensive Linkage and Genetic Coupling of Song and Preference Loci Underlying Rapid Speciation in Laupala Crickets

Abstract In nature, closely related species commonly display divergent mating behaviors, suggesting a central role for such traits in the origin of species. Elucidating the genetic basis of divergence in these traits is necessary to understand the evolutionary process leading to reproductive barriers and speciation. The rapidly speciating Hawaiian crickets of the genus Laupala provides an ideal system for dissecting the genetic basis of mating behavior divergence. In Laupala, closely related species differ markedly in male song pulse rate and female preference for pulse rate. These behaviors play an important role in determining mating patterns. Previous studies identified a genetic architecture consisting of numerous small to moderate effect loci causing interspecific differences in pulse rate and preference, including colocalizing pulse rate and preference QTL on linkage group one (LG1). To further interrogate these QTL, we conduct a fine mapping study using high-density SNP linkage maps. With improved statistical power and map resolution, we provide robust evidence for genetic coupling between song and preference, along with two additional pulse rate QTL on LG1, revealing a more resolved picture of the genetic architecture underlying mating behavior divergence. Our sequence-based genetic map, along with dramatically narrowed QTL confidence intervals, allowed us to annotate genes within the QTL regions and identify several exciting candidate genes underlying variation in pulse rate and preference divergence. Such knowledge suggests potential molecular mechanisms underlying the evolution of behavioral barriers.