Sexual Signal Divergence and Reproductive Isolation in an Adaptive Radiation of a Hawaiian Spider

Abstract Adaptive radiations have long served as key models for understanding the process of speciation, yet the relative timing and role of ecological vs sexual divergence in the rapid formation of reproductive isolation remains unclear. Many of the sexual signaling traits shown to play a key role in adaptive radiations are deeply intertwined with the ecological factors that power the ecological divergence and hence there is still much uncertainty as to how these sexual traits themselves drive diversification. Using a combination of chemical, behavioral, and genetic data, this study investigates the role of chemical sexual signals in Tetragnatha quasimodo, a species within an adaptive radiation of Hawaiian spiders, where populations are genetically divergent yet maintain similar niches. We find that the chemical signals of these spiders vary substantially with four distinct chemical profiles (chemotypes) that were not associated with measured environmental factors nor genetic distance. Behavioral trials showed strong assortative mate preference with males significantly choosing the same chemotype as themselves over other different chemotypes. There was substantial genetic differentiation between chemotypes, and individuals of a specific chemotype were more closely related to different chemotypes on the same island than to the same chemotype on different islands. Lastly, on the youngest island (Hawai’i), chemical differences were found in populations that were genetically similar, suggesting the possibility that sexual signal divergence can evolve before genetic divergence. These findings provide key insights into the role chemical sexual signals play in the attainment and maintenance of reproductive barriers in isolation of the ecological divergence found in this lineage.