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Dryad

Linked song and preference loci suggest substantial contribution of genetic coupling in rapid speciation of the Laupala crickets

Abstract

Species-specific sexual signals and preferences are central to the evolutionary origins and maintenance of reproductive barriers. How such communication systems evolve is key to understanding speciation. One central question considers how signals and preferences coevolve within lineages while each diverges among lineages. Here, we study the rapidly speciating Laupala cricket, a system characterized by coordinated sexual signaling. By fine-mapping variation for both the pulse rate of the male calling song and female pulse rate preference, we examine the genetic architecture underlying signal-preference divergence. We document a pair of colocalizing pulse rate and preference QTL on linkage group 4, with peak locations less than 2 cM apart, offering strong evidence for genetic coupling. Intriguingly, this is the third pair of colocalizing male and female loci mapped in the Laupala genome. The cumulative effect size of the three pairs of colocalizing loci accounts for roughly half of the interspecific difference, suggesting that genetic coupling has contributed substantially to the evolution of this behavioral barrier in Laupala. Annotation of the QTL region identified numerous functionally relevant candidate genes, including acetylcholine esterase (AChE) and ryanodine receptor (RyR).