Sanders, KateSimões, BrunoRossetto, Isaac Henry2024-07-262024-07-262024https://hdl.handle.net/2440/141674Fully-marine sea snakes share a recent terrestrial ancestor with Australian elapid snakes, yet the sensory adaptations that accompanied this land-sea transition are largely unknown. The spectral conditions of marine environments vary to a far greater degree than that of terrestrial environments, meaning that the visual systems of secondarily-aquatic species are likely to undergo large-scale adaptive change during transition. My thesis explored the visual evolution of a group of hydrophiine snakes, and compared this with that of their terrestrial relatives. A wide variety of molecular and histological methods were used to investigate the genomic basis and function of adaptive specialisations in the sea snake eye. Previous studies have shown that some sea snakes have expanded “UV-blue” spectral sensitivity via adaptive changes to their Short-Wavelength-Sensitive-Opsin-1 gene. Chapter 2 of this thesis instead suggested that some sea snake species of the Hydrophis genus possess multiple SWS1 visual opsin genes. Gene duplications of this nature are of high evolutionary significance, as the advanced visual ability observed throughout much of the animal kingdom evolved via duplications of photopigment-encoding opsin genes and subsequent shifts in wavelength sensitivity of the copies. Though significant, these duplication events are also incredibly rare; with only three occurrences within the last ~400 million years of tetrapod evolution having been confirmed outside of the current study. To investigate the potential for functional expansion of the opsin repertoire in Hydrophis, we compared the spectral tuning nucleotide sites between gene copies. This led to the discovery of divergence at a key spectral tuning site, which likely means that some SWS1 copies allow for the retinal perception of blue-light spectra, while other copies allow for UV-light perception. It is therefore possible that this rare case of gene duplication has enabled sea snakes to shift from ancestrally dichromatic to trichromatic vision during their adaptation to marine life. The rarity of visual opsin expansion in tetrapod lineages prompted us to further investigate this unlikely duplication of the SWS1 gene in Hydrophis sea snakes. Chapter 3 expanded the known list of sea snake species with expanded opsin repertoires by generating one new genome, 45 resequencing datasets and 81 SWS1 exon 1 sequences, and analysed these alongside 16 existing genomes for sea snakes and their terrestrial relatives. This revealed the presence of multiple SWS1 genes in H. cyanocinctus, H. spiralis, H. melanocephalus, H. curtus, H. atriceps and H. fasciatus. The phylogenetic distribution of SWS1 variants suggested that multiple independent and convergent expansion events have caused the variation in gene copy number observed throughout Hydrophis. To test the functional potential of SWS1 subtypes we generated 10 retinal transcriptomes, and found that both UV- and blue-sensitive variants were expressed within the retinae of both H. cyanocinctus and H. atriceps. This suggested that this case of expansion likely confers a novel phenotype; potentially even trichromacy. In Chapter 4, we compared the genomic presence and transcriptomic expression of 50 key vision-associated genes in a range of species spanning the snake phylogeny. We found little variation in the repertoires of visual genes between terrestrial, semi-aquatic and fully-marine species. We then investigated the sea snake retina for evidence of adaptive specialisation to the marine photic environment. Photoreceptor morphology and ultrastructure was explored in species belonging to two major clades of sea snake; Hydrophis and Aipysurus. We identified the presence of rod photoreceptors exclusive to Aipysurus which have likely transmuted from the rod-like cones found in both sister clades, thereby highlighting a remarkable case of divergent sensory evolution following an ancestral land-sea transition. We also investigated expression of visual opsins within these photoreceptors using immunohistochemistry. The RH1 and SWS1 opsins were discovered to be coexpressed within single cone photoreceptors in various species of Hydrophis. Coexpression of these opsin types has not been reported in any vertebrate species, and may be exclusive to these fully-marine snakes. The collective findings presented in this thesis have enhanced our understanding of visual evolution following dramatic ecological transitions. The complex retinal adaptations developed by sea snakes is a striking contrast to the visual regression observed in other secondarily-aquatic groups, including cetaceans, pinnipeds and penguins.enevolutionvisionsensory systemssnakessea snakemolecular biologyThesis