Evolution of the non-visual and visual opsin gene repertoire in ray-finned fishes

Abstract

Photoreception - the detection of light for image formation (vision) as well as for non-image-forming purposes (circadian regulation, 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 non-visual opsins. Here, we provide the most comprehensive study to date on the evolution of the opsin gene family in the largest class of vertebrate, fishes, with a particular focus on the understudied non-visual 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 non-visual opsins. We provide compelling evidence that visual and non-visual opsins co-evolve 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 all in the dark (such as in caves or the deep sea) convergently reduced their visual and non-visual opsin gene repertoires, while polar species feature accelerated evolution in both. Fishes that rely on electroreception show a reduction in the number of visual and non-visual opsin genes and accelerated evolution of the remaining genes. We further found that genes of the phototransduction cascade co-evolve with opsins. Finally, that non-visual opsins are mainly expressed in testes and ovaries (next to the eyes) supports a function in gamete biology.