Sink or swim: Phylogenomic analysis of Baikal sculpins reveals multiple transformations to pelagic, bathybenthic, and lotic ecomorphologies

Lake Baikal ranks among the world's most species-rich freshwater ecosystems; however, the evolutionary histories of endemic taxa remain poorly understood. The unique abiotic environments of Lake Baikal include the only bathybenthic, bathypelagic, and deep hydrothermal vent communities in freshwater, each of which supports species with derived morphological and physiological traits. As the only known vertebrate radiation endemic to a non-tropical ancient lake, Baikal sculpins represent an underappreciated resource for investigating evolutionary processes that underlie adaptive radiation. We examined morphological and ecological diversity among Baikal sculpins and present the first interspecific phylogeny inferred from dense nuclear genomic sampling (ddRADseq). The new phylogeny supports a holarctic lotic ancestor to a limnetic radiation and reveals reticulate adaptations to lotic, bathyal, and pelagic habitats. We apply the new phylogeny to revise Baikal sculpin taxonomy, and we resurrect Uranidea as a monotypic sister-group to the Baikal sculpin radiation. Our data support independent evolution of pelagic and bathypelagic ecomorphs and multiple invasions of aphotic habitats. Concordant ecomorphological shifts involved dramatic modification of skeletal elements, sensory systems, and reproductive mode. Habitat depth is highlighted as an important abiotic factor associated with adaptive radiation, but more research is needed to address potentially confounding effects of thermal and photic zonation. We discuss the geoclimatic processes that may explain this rapid radiation, and conclude by highlighting the anthropogenic changes that threaten this irreplaceable natural resource.