Characterization and Evolution of the Spotted Gar Retina

Abstract

In this study we characterize the retina of the spotted gar, Lepisosteus oculatus, a ray-finned fish. Gar did not undergo the whole genome duplication event that occurred at the base of the teleost fish lineage, which includes the model species zebrafish and medaka. The divergence of gars from the teleost lineage and the availability of a high quality genome sequence make it a uniquely useful species to understand how genome duplication sculpted features of the teleost visual system, including photoreceptor diversity. We developed reagents to characterize the cellular organization of the spotted gar retina, including representative markers for all major classes of retinal neurons and Müller glia. We report that the gar has a preponderance of predicted short-wavelength (SWS) shifted opsin genes, including a duplicated set of SWS1 (ultraviolet) sensitive opsin encoding genes, a SWS2 (blue) opsin encoding gene, and two rod opsin encoding genes, all of which were expressed in retinal photoreceptors. We also report that gar SWS1 cones lack the geometric organization of photoreceptors observed in teleost fish species, consistent with the crystalline photoreceptor mosaic being a teleost innovation. Of note the spotted gar expresses both exo-rhodopsin (RH1-1) and rhodopsin (RH1-2) in rods. Exo-rhodopsin is an opsin that is not expressed in the retina of zebrafish and other teleosts, but rather is expressed in regions of the brain. This study suggests that exo-rhodopsin is an ancestral actinopterygian (ray finned fish) retinal opsin, and in teleosts its expression has possibly been subfunctionalized to the pineal gland.

The non‐visual opsins: eighteen in the ancestor of vertebrates, astonishing increase in ray‐finned fish, and loss in amniotes

“…This naming proposal is also similar to another; Sukeena et al. () recommended that fish Exorh be changed to Rh1‐1 based upon the discovery that its expression is not exclusively “extra‐ocular” (“Exo”) after all. The neuropsins are often called Opn5 genes.…”

“…Beyond a phylogenetic motivation for the name change, all of these genes were shown to occur in non-teleosts. This naming proposal is also similar to another; Sukeena et al (2016) recommended that fish Exorh be changed to Rh1-1 based upon the discovery that its expression is not exclusively "extra-ocular" ("Exo") after all. The neuropsins are often called Opn5 genes.…”

“…Figure S1). Most ray‐finned fish have two Rho homologs, Exorh and Rho, which were recently renamed Rh1‐1 and Rh1‐2, respectively (Sukeena et al., ). The ray‐finned fish Rho (Rh1‐2) clade is derived from a retro‐duplication event in the ancestor of Actinopteri (Bellingham, Tarttelin, Foster, & Wells, ) and our phylogenetic analysis generated a tree topology consistent with this duplication history (Suppl.…”

“…Also intriguing was the discovery of pinopsin in spotted gar, but not in any other ray‐finned fish surveyed (see Braasch et al., ; Sukeena et al., ). Genomes are believed to go through a period of great instability after whole‐genome duplication events and this instability includes large‐scale gene loss (Semon and Wolfe, ).…”

The Spotted Gar: Genomic Journeys into a Lost World

“…Beaudry et al (2017) used the spotted gar genome as starting point to illuminate the evolutionary history of non-visual opsin genes among vertebrates. The spotted gar retina and its visual opsins had been recently characterized in an earlier publication in JEZB (Sukeena et al, 2016).…”