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

Abstract

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 marineHydrophisclade, with at least three lineages having multiple intact SWS1 genes: the previously studiedHydrophis cyanocinctusand at least two close relatives of this species;H. atriceps-H. fasciatus;and an individualH. 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 ofH. cyanocinctusandH. 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.SignificanceSecondary transitions to marine environments are commonly accompanied by pseudogenisation of the visual opsin genes which mediate colour perception. Conversely, a species of fully-marine hydrophiid snake has functionally expanded its short-wavelength-sensitive opsin repertoire following a terrestrial ancestry. The current study explores this further by mapping opsin copy number across the hydrophiid phylogeny and by quantifying expression of SWS1 subtypes within sea snake retinae. Despite few reports of opsin expansions in tetrapods, we provide evidence for the occurrence of multiple expansion events throughoutHydrophis. Most intriguingly, retinal expression of spectrally-divergent copies implies a functionally-significant phenotype; possibly even trichromacy.