Phylogenetic mapping of sleep loss in wild-caught cavefish

Sleep is an evolutionarily ancient and nearly universal behavior throughout the animal kingdom. Multiple cave-dwelling populations of the Mexican tetra, Astyanax mexicanus , have converged on sleep loss compared to river dwelling surface fish. However, the extent to which sleep has been lost across cave populations, and whether sleep loss occurs in wild fish, is poorly understood. We have measured sleep and locomotor activity in 15 distinct populations of A. mexicanus representing multiple lineages that are broadly representative of the 34 cavefish populations identified to date. Strikingly, sleep was largely lost in all cave and hybrid populations that were tested. Hybrid populations retained intermediate eye and pigmentation phenotypes, suggesting sleep loss precedes cave-associated morphological changes. Mapping behavioral changes onto the phylogeny of A. mexicanus populations revealed that independent loss of sleep and elevated locomotor activity has occurred at least three times. Analysis of sleep in the wild confirms that the sleep loss phenotype observed in lab-reared fish is also present in the natural environment. Together, these findings reveal deep evolutionary convergence on sleep loss in cavefish and provide evidence for sleep loss as a primary trait contributing to cave adaptation.