Hybridization underlies localized trait evolution in cavefish

A rapidly growing body of work has demonstrated that introgressive hybridization often drives patterns of phenotypic evolution and may play an integral role in the evolutionary processes of local adaptation and speciation. Indeed, several of studies have shown that behavioral variation can result from introgressive hybridization (e.g., song in hybrid Darwin’s finches, mate choice in hybrid baboons, defensive behavior in hybrid honey bees), providing new substrate for selection to act upon. A powerful model system for investigating the genetic and evolutionary basis of trait development and behavior is the Mexican tetra, Astyanax mexicanus. Cave populations have repeatedly evolved numerous traits including eye loss, sleep loss, and albinism. Of the 30 caves inhabited by A. mexicanus, the Chica cave is unique because it contains several pool microenvironments inhabited by putative hybrids between surface and cave populations, providing an opportunity to investigate hybridization and its impact on complex trait evolution. We demonstrate that hybridization between cave and surface populations contributes to highly localized variation in pigmentation, eye development, and sleep, traits that are thought to be associated with cave evolution. Our findings suggest that hybridization drives highly-localized behavioral and morphological evolution. Lastly, our analyses uncovered a compelling example of convergent evolution in a core circadian clock gene in multiple independent cavefish lineages and burrowing mammals, suggesting a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Together, our results provide insight into the evolutionary mechanisms that generate adaptive genetic variation.