Evolution of Pineal Nonvisual Opsins in Lizards and the Tuatara and Identification of Lepidopsin: A New Opsin Gene

Many lizards (Squamata), as well as the tuatara (Rhynchocephalia), are distinguished among vertebrate groups for the presence of the parietal eye, or "third eye", a structure derived from the pineal complex containing a simplified retina with photoreceptor cells. The parietal eye expresses nonvisual opsins that differ from the visual opsin repertoire of the lateral eyes. These are pinopsin (OPNP), parapinopsin (OPNPP), and parietopsin (OPNPT), all being evolutionary close to visual opsins. Here, we searched over 60 lepidosaurian genomes for pineal nonvisual opsins to check for the evolutionary trajectory of these genes in reptiles. Unexpectedly, we identified a novel opsin gene, which we termed "lepidopsin" (OPNLEP), that is present solely in the genomes of the tuatara and most lizard groups but absent from other vertebrates. Remnants of the gene are found in the coelacanth and some ray-finned fishes, implying that OPNLEP is an ancient opsin that has been repeatedly lost during vertebrate evolution. We found that the tuatara and most lizards of the Iguania, Anguimorpha, Scincoidea, and Lacertidae clades, which possess a parietal eye, harbor all pineal opsin genes. Lizards missing the parietal eye, like geckos, teiids, and a fossorial amphisbaenian, lack most or all pineal nonvisual opsins. In summary, our survey of pineal nonvisual opsins reveals (i) the persistence of a previously unknown ancient opsin gene-OPNLEP-in lepidosaurians; (ii) losses of nonvisual opsins in specific lizard clades; and (iii) a correlation between the presence of a parietal eye and the genomic repertoire of pineal nonvisual opsins.