Metazoan opsin evolution reveals a simple route to animal vision

Abstract

All known visual pigments in Neuralia (Cnidaria, Ctenophora, and Bilateria) are composed of an opsin (a seven-transmembrane G protein-coupled receptor), and a light-sensitive chromophore, generally retinal. Accordingly, opsins play a key role in vision. There is no agreement on the relationships of the neuralian opsin subfamilies, and clarifying their phylogeny is key to elucidating the origin of this protein family and of vision. We used improved methods and data to resolve the opsin phylogeny and explain the evolution of animal vision. We found that the Placozoa have opsins, and that the opsins share a common ancestor with the melatonin receptors. Further to this, we found that all known neuralian opsins can be classified into the same three subfamilies into which the bilaterian opsins are classified: the ciliary (C), rhabdomeric (R), and go-coupled plus retinochrome, retinal G protein-coupled receptor (Go/RGR) opsins. Our results entail a simple scenario of opsin evolution. The first opsin originated from the duplication of the common ancestor of the melatonin and opsin genes in a eumetazoan (Placozoa plus Neuralia) ancestor, and an inference of its amino acid sequence suggests that this protein might not have been light-sensitive. Two more gene duplications in the ancestral neuralian lineage resulted in the origin of the R, C, and Go/RGR opsins. Accordingly, the first animal with at least a C, an R, and a Go/RGR opsin was a neuralian progenitor.

Fig. 1.

Phylogeny of the opsin family. (A) Unrooted phylogeny of the neuralian opsins. (B) Rooted phylogeny of the neuralian opsins and of other GPCRs showing that the Placopsins are members of the opsin family (Ore, orexin; Lys, lysosphingolipid). (C) Opsin phylogeny rooted by using only the MLT receptors, and showing that cnidarians have orthologues of each bilaterian opsin subfamily: the C, R, and Go/RGR subfamilies. Support values (Bayesian PPs) are reported only for key nodes (SI Appendix shows all support values). The ancestral RBD of the LOCA and of the LOCNA are reported and are identified, respectively, by a black star and a black circle (SI Appendix, Fig. S7). The red position in the logos identifies position 296.

Fig. 2.

Synopsis of opsin evolution. This figure represents a gene tree embedded within a species tree illustrating the evolutionary history of the opsins and MLT receptors in Metazoa. It shows that only three duplications and no deletions are necessary to explain opsin evolution.