Parallel Spectral Tuning of a Cone Visual Pigment Provides Evidence for Ancient Deep-Sea Adaptations in Cetaceans

Dichromatic color vision is mediated by two cone visual pigments in many eutherian mammals. After reentry into the sea, early cetaceans lost their violet-sensitive visual pigment (short wavelength-sensitive 1) independently in the baleen and toothed whale ancestors and thus obtained only monochromatic cone vision. Subsequently, losses of the middle/long wavelength-sensitive (M/LWS) pigment have also been reported in multiple whale lineages, leading to rhodopsin (RH1)-mediated rod monochromatic vision. To further elucidate the phenotypic evolution of whale visual pigments, we assessed the spectral tuning of both M/LWS and RH1 from representative cetacean taxa. Interestingly, although the coding sequences for M/LWS are intact in both the pygmy right whale and the Baird's beaked whale, no spectral sensitivity was detected in vitro. Pseudogenization of other cone vision-related genes is observed in the pygmy right whale, suggesting a loss of cone-mediated vision. After ancestral sequence reconstructions, ancient M/LWS pigments from cetacean ancestors were resurrected and functionally measured. Spectral tuning of M/LWS from the baleen whale ancestor shows that it is green sensitive, with a 40-nm shift in sensitivity to a shorter wavelength. For the ancestor of sperm whales, although no spectral sensitivity could be recorded for its M/LWS pigment, a substantial sensitivity shift (20 to 30 nm) to a shorter wavelength may have also occurred before its functional inactivation. The parallel phenotypic evolution of M/LWS to shorter wavelength sensitivity might be visual adaptations in whales allowing more frequent deep-sea activities, although additional ecological differentiations may have led to their subsequent losses.