The evolution of the green-light-sensitive visual opsin genes (RH2) in teleost fishes

Vertebrates have four visual cone opsin classes that mediate sensitivity from ultraviolet to red wavelengths of light. The rhodopsin-like 2 (RH2) opsin is sensitive to the central mostly green part of the spectrum. While lost in some terrestrial vertebrates (mammals), the RH2 opsin gene has proliferated during the evolution of teleost fishes. Here, we investigated the genomes of 132 extant teleosts and found between zero and eight RH2 gene copies per species. The RH2 gene shows a dynamic evolutionary history with repeated gene duplications, gene losses, and gene conversions affecting entire orders, families, and species. At least four ancestral duplications provided the substrate for today's RH2 diversity, with duplications occurring in the common ancestors of Clu-peocephala (twice), Neoteleostei, and likely Acanthopterygii as well. Despite these evolutionary dynamics, we identified conserved RH2 synteny in two main gene clusters; the slc6A13/synpr cluster is highly conserved within Percomorpha and also present across most teleosts, including Otomorpha, Euteleostei and in parts in tarpons (Elopomorpha), and the mutSH5 cluster, which is specific for Otomorpha. When comparing the number of visual opsin genes (SWS1, SWS2, RH2, LWS, and total cone opsins) with habitat depth, we found that deeper-dwelling species had less (or none) long-wavelength-sensitive opsins. Using retinal/eye transcriptomes in a phylogenetic representative dataset of 32 species, we show that if present in the genome, RH2 is expressed in most fishes except for some species within the tarpons, characins, and gobies (and Osteoglossomorpha and some other characin species have lost the gene). Those species instead express a green-shifted long-wavelength-sensitive LWS opsin. Our study applies modern genomic and transcriptomic tools within a comparative framework to elucidate the evolutionary history of the visual sensory system in teleost fishes.

Automated summary

Vertebrates have evolved four visual cone opsin classes that allow sensitivity to different wavelengths of light. The RH2 opsin, which is sensitive to green light, has undergone gene duplications, losses, and conversions in the evolution of teleost fishes. By studying the genomes and retinal/eye transcriptomes of 132 teleost species, researchers found a varying number of RH2 gene copies per species and identified conserved gene clusters. The study also revealed a correlation between habitat depth and the presence of certain opsin genes in the visual system of teleost fishes.