Adaptive loss of shortwave-sensitive opsins during cartilaginous fish evolution

Abstract

Cartilaginous fishes (e.g., sharks, rays, and skates) cannot see blue or violet light, potentially because they lack the shortwave-sensitive cone opsin gene (sws). Widespread gene loss can occur during evolution, but the evolutionary mechanisms underlying sws loss remains unclear. Here, we construct whole-genome assemblies of Okamejei kenojei (skate) and Prionace glauca (blue shark). We then analyze the distribution characteristics and intragroup differences of opsin-related genes in cartilaginous fishes. Using a zebrafish model with sws deleted we infer that in the presence of SWS1 and SWS2, blue and violet light respectively, can induce cell aging. This is followed by photoreceptor layer thinning, demonstrating, sws loss aids in preventing shortwave light damage to the eye. In the retinas of numerous cartilaginous fishes, the tapetum lucidum strongly reflects light. Therefore, in cartilaginous fish, the existence of tapetum lucidum in the retina and loss of sws may be interdependent; in other words, this adaptive gene loss may increase cartilaginous fish fitness.