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.

Sea snake harvest in the gulf of Thailand.

Conservation of sea snakes is virtually nonexistent in Asia, and its role in human-snake interactions in terms of catch, trade, and snakebites as an occupational hazard is mostly unexplored. We collected data on sea snake landings from the Gulf of Thailand, a hotspot for sea snake harvest by squid fishers operating out of the ports of Song Doc and Khanh Hoi, Ca Mau Province, Vietnam. The data were collected during documentation of the steps of the trading process and through interviewers with participants in the trade. Squid vessels return to ports once per lunar synodic cycle and fishers sell snakes to merchants who sort, package, and ship the snakes to various destinations in Vietnam and China for human consumption and as a source of traditional remedies. Annually, 82 t, roughly equal to 225,500 individuals, of live sea snakes are brought to ports. To our knowledge, this rate of harvest constitutes one of the largest venomous snake and marine reptile harvest activities in the world today. Lapemis curtus and Hydrophis cyanocinctus constituted about 85% of the snake biomass, and Acalyptophis peronii, Aipysurus eydouxii, Hydrophis atriceps, H. belcheri, H. lamberti, and H. ornatus made up the remainder. Our results establish a quantitative baseline for characteristics of catch, trade, and uses of sea snakes. Other key observations include the timing of the trade to the lunar cycle, a decline of sea snakes harvested over the study period (approximately 30% decline in mass over 4 years), and the treatment of sea snake bites with rhinoceros horn. Emerging markets in Southeast Asia drive the harvest of venomous sea snakes in the Gulf of Thailand and sea snake bites present a potentially lethal occupational hazard. We call for implementation of monitoring programs to further address the conservation implications of this large-scale marine reptile exploitation.