Genetic coupling of signal and preference facilitates sexual isolation during rapid speciation.

Abstract

The divergence of sexual signals is ultimately a coevolutionary process: while signals and preferences diverge between lineages, they must remain coordinated within lineages for matings to occur. Divergence in sexual signals makes a major contribution to evolving species barriers. Therefore, the genetic architecture underlying signal-preference coevolution is essential to understanding speciation but remains largely unknown. In Laupala crickets where male song pulse rate and female pulse rate preferences have coevolved repeatedly and rapidly, we tested two contrasting hypotheses for the genetic architecture underlying signal-preference coevolution: linkage disequilibrium between unlinked loci and genetic coupling (linkage disequilibrium resulting from pleiotropy of a shared locus or tight physical linkage). Through selective introgression and quantitative trait locus (QTL) fine mapping, we estimated the location of QTL underlying interspecific variation in both female preference and male pulse rate from the same mapping populations. Remarkably, map estimates of the pulse rate and preference loci are as close as 0.06 cM apart, the strongest evidence to date for genetic coupling between signal and preference loci. As the second pair of colocalizing signal and preference loci in the Laupala genome, our finding supports an intriguing pattern, pointing to a major role for genetic coupling in the quantitative evolution of a reproductive barrier and rapid speciation in Laupala. Owing to its effect on suppressing recombination, a coupled, quantitative genetic architecture offers a powerful and parsimonious genetic mechanism for signal-preference coevolution and the establishment of positive genetic covariance on which the Fisherian runaway process of sexual selection relies.