Genomic linkage of male song and female acoustic preference QTL underlying a rapid species radiation

The genetic coupling hypothesis of signal-preference evolution, whereby the same genes control male signal and female preference for that signal, was first inspired by the evolution of cricket acoustic communication nearly 50 years ago. To examine this hypothesis, we compared the genomic location of quantitative trait loci (QTL) underlying male song and female acoustic preference variation in the Hawaiian cricket genus Laupala. We document a QTL underlying female acoustic preference variation between 2 closely related species (Laupala kohalensis and Laupala paranigra). This preference QTL colocalizes with a song QTL identified previously, providing compelling evidence for a genomic linkage of the genes underlying these traits. We show that both song and preference QTL make small to moderate contributions to the behavioral difference between species, suggesting that divergence in mating behavior among Laupala species is due to the fixation of many genes of minor effect. The diversity of acoustic signaling systems in crickets exemplifies the evolution of elaborate male displays by sexual selection through female choice. Our data reveal genetic conditions that would enable functional coordination between song and acoustic preference divergence during speciation, resulting in a behaviorally coupled mode of signal-preference evolution. Interestingly, Laupala exhibits one of the fastest rates of speciation in animals, concomitant with equally rapid evolution in sexual signaling behaviors. Genomic linkage may facilitate rapid speciation by contributing to genetic correlations between sexual signaling behaviors that eventually cause sexual isolation between diverging populations.