Evolutionary Transitions Drive Molecular Adaptation in Sculpin Rhodopsin

Evolutionary habitat transitions are known to drive rapid evolution. In fishes, switches between marine and freshwater can promote adaptation in sensory systems; in particular, the disparate visual environments in these aquatic habitats can lead to evolution at all levels of the visual system. We investigate the evolution of dim light-sensitive rhodopsin genes within the sculpin (Cottoidea), a species-rich group of fishes occupying diverse benthic habitats. Two main families include Psychrolutidae, occupying marine waters from shallow coastal to the deep sea, and Cottidae, including both a freshwater radiation of shallow-dwelling species and the flock of endemic Lake Baikal sculpin. We used molecular evolution models to define the selective pressures acting on cottoid rhodopsin genes and estimated the spectral absorbance of rhodopsin proteins across this group, hypothesizing that numerous habitat transitions have generated functional diversity within cottoid rhodopsin. Our findings indicate pervasive positive selection across sculpin rhodopsin. The freshwater transition and subsequent radiation throughout Holarctic freshwaters promoted significant genetic diversification and appears to have led to a strongly red-shifted spectral absorbance, while the sculpin of Lake Baikal evolved numerous mutations to progressively blue-shift rhodopsin as they adapted to increasingly deep waters. The rhodopsin genes of the marine Psychrolutidae are also under strong positive selection, although spectral absorbance does not appear to correlate with habitat depth. Instead, non-spectral adaptation of rhodopsin to facilitate dim-light vision throughout a migratory life history may be driving, and constraining, evolution.