An Extensive Survey of Vertebrate-specific, Nonvisual Opsins Identifies a Novel Subfamily, Q113-Bistable Opsin

A group of nonvisual opsins specific to vertebrates is essential to understand evolution of lateral eyes, one of the most prominent innovations in this lineage. Nevertheless, our knowledge of their evolutionary history remains limited. To develop an integrated view of their evolution, we surveyed these non-visual opsins (VA opsin, pinopsin, parapinopsin, parietopsin, and parapinopsin-like) in 451 vertebrate genomes. Through extensive manual curation, we completed a high-quality catalog. We could not find them in 202 mammals, supporting previous reports of their loss. VA opsins are highly conserved among nonmammals. In contrast, other opsin subfamilies experienced more dynamic molecular evolution with many secondary losses. In addition, we found a previously unreported opsin subfamily that we named Q113-Bistable (QB) opsin. We found its orthologs only in several lizards and the tuatara. Nevertheless, QB opsin pseudogenes were discovered in diverse taxa, including ray-finned fishes, indicating its ancient origin. QB opsin, parapinopsin, and parietopsin are extremely prone to be lost in the course of evolution, and loss events involving these opsins seem to occur concomitantly. Furthermore, we demonstrated the spectral properties of QB opsin as a UV-sensitive, bistable photo-pigment. This study provides the first integrated view of the entire evolutionary history of this group of opsins.