Evolution of the Nonvisual and Visual Opsin Gene Repertoire in Ray-Finned Fishes

Photoreception-the detection of light for image formation (vision) as well as for nonimage-forming purposes (circadian regulation and DNA repair)-is critical to the survival of most animals. In vertebrates, photoreception is mediated by opsin proteins, which are classified, according to their function, into visual and nonvisual opsins. Here, we provide the most comprehensive study to date on the evolution of the opsin gene family in the largest class of vertebrates, actinopterygians, with a particular focus on the understudied nonvisual opsins. Based on an in-depth analysis of 535 high-quality genomes, we document great variation in gene numbers in the different opsin gene subfamilies across ray-finned fishes and show that visual opsins are more prone to duplications and losses than nonvisual opsins. We provide evidence that visual and nonvisual opsins coevolve in ray-finned fishes, both in terms of copy numbers and selective pressures acting on their coding sequences, probably in response to the different photic environments they inhabit. Species that live in dim light or in the dark (such as in caves or the deep sea) had reduced visual and nonvisual opsin gene repertoires, while polar species feature accelerated evolution in both. Fishes that rely on electroreception show a slight reduction in the number of visual and nonvisual opsin genes and accelerated evolution of the remaining genes. We further found that genes of the phototransduction cascade coevolve with opsins. Finally, the finding that nonvisual opsins are mainly expressed in the testes and ovaries (after the eyes) supports a function in gamete biology.