Dynamic Expansions and Retinal Expression of Spectrally Distinct Short-Wavelength Opsin Genes in Sea Snakes.

The photopigment-encoding visual opsin genes that mediate colour perception show great variation in copy number and adaptive function across vertebrates. An open question is how this variation has been shaped by the interaction of lineage-specific structural genomic architecture and ecological selection pressures. We contribute to this issue by investigating the expansion dynamics and expression of the duplicated Short-Wavelength-Sensitive-1 opsin (SWS1) in sea snakes (Elapidae). We generated one new genome, 45 resequencing datasets, 10 retinal transcriptomes, and 81 SWS1 exon sequences for sea snakes, and analysed these alongside 16 existing genomes for sea snakes and their terrestrial relatives. Our analyses revealed multiple independent transitions in SWS1 copy number in the marine Hydrophis clade, with at least three lineages having multiple intact SWS1 genes: the previously studied Hydrophis cyanocinctus and at least two close relatives of this species; H. atriceps-H. fasciatus; and an individual H. curtus. In each lineage, gene copy divergence at a key spectral tuning site resulted in distinct UV and Violet/Blue-sensitive SWS1 subtypes. Both spectral variants were simultaneously expressed in the retinae of H. cyanocinctus and H. atriceps, providing the first evidence that these SWS1 expansions confer novel phenotypes. Finally, chromosome annotation for nine species revealed shared structural features in proximity to SWS1 regardless of copy number. If these features are associated with SWS1 duplication, expanded opsin complements could be more common in snakes than is currently recognised. Alternatively, selection pressures specific to aquatic environments could favour improved chromatic distinction in just some lineages.

Functional Duplication of the Short-Wavelength-Sensitive Opsin in Sea Snakes: Evidence for Reexpanded Color Sensitivity Following Ancestral Regression.

Color vision is mediated by ancient and spectrally distinct cone opsins. Yet, while there have been multiple losses of opsin genes during the evolution of tetrapods, evidence for opsin gains via functional duplication is extremely scarce. Previous studies have shown that some secondarily marine elapid snakes have acquired expanded "UV-blue" sensitivity via changes at key spectral tuning amino acid sites of the Short-Wavelength Opsin 1 (SWS1) gene. Here, we use elapid reference genomes to show that the molecular origin of this adaptation involved repeated, proximal duplications of the SWS1 gene in the fully marine Hydrophis cyanocinctus. This species possesses four intact SWS1 genes; two of these genes have the ancestral UV sensitivity, and two have a derived sensitivity to the longer wavelengths that dominate marine habitats. We suggest that this remarkable expansion of the opsin repertoire of sea snakes functionally compensates for the ancestral losses of two middle-wavelength opsins in the earliest (dim-light adapted) snakes. This provides a striking contrast to the evolution of opsins during ecological transitions in mammals. Like snakes, early mammals lost two cone photopigments; however, lineages such as bats and cetaceans underwent further opsin losses during their adaptation to dim-light environments.