Evolutionary Genomics of an Adaptive Radiation: Viviparous Sea Snakes (Elapidae)

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2023

Authors

Ludington, Alastair John

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Sanders, Kate
Breen, James (Telethon Kids Institute, John Curtin School of Medical Research, College of Health & Medicine, ANU)

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Abstract

Viviparous sea snakes (Hydrophiinae; Elapidae) underwent a dramatic and remarkably recent transition from land to sea in the last 10 million years, yet they remain a conspicuous gap in molecular studies of speciation and adaptation in vertebrates. My thesis addresses this knowledge gap by generating new high-quality genomic resources for sea snakes and analysing these data, alongside existing datasets, to understand the demographic and genetic basis of ecological transitions and rapid radiation within elapid snakes. Marine systems are often suggested to support large, highly connected populations, but quantitative comparisons with terrestrial systems have been lacking. Further, it has been shown that co-occurring species often have congruent responses to past ecological events. Genomes of organisms contain a record of their evolutionary and ecological past, and as such can shed light on species’ responses to past biotic and abiotic factors. Using coalescent methods and whole genome data, I compared the effective population sizes between seven terrestrial and marine elapids. The results of this analysis found that, contrary to expectation, effective population sizes in marine species were not larger, instead showing highly variable patterns that did not clearly correspond with major ecological divisions. This work provided one of the first preliminary studies comparing terrestrial and marine elapids, providing the basis for future demographic studies looking to understand the role of ecological and biogeographic factors in shaping population dynamics. nderstanding the genetic basis of the terrestrial-to-marine transition in sea snakes remains a prominent gap in studies of marine adaptation in vertebrates. Using newly generated chromosome-scale reference genomes, representing the most complete genomes available for Elapidae, I performed comparative genomic analyses between six Hydrophis sea snakes and seven terrestrial snakes. Through phylogenomic analyses, we highlight the possibility of reticulate speciation at the root of Hydrophis, while whole genome alignments elucidate extensive chromosomal synteny within Hydrophis, identifying structural variations that will be key candidates for future studies. Finally, I used a strict screen for positive selection to identify adaptive candidate genes in Hydrophis, relative to the terrestrial background, which showed over-representation for hypoxia adaptation, sensory perception, and morphological development. Finally, genome scans were used to explore the divergence profiles between three ecologically distinct and coexisting species that diverged near-simultaneously 3-8 million years ago. Our results support early admixture between the three species, in addition to shared evolutionary processes that likely shaped their conserved genomic landscapes. Numerous islands of divergence were identified, whose profiles best fit a scenario of long-term linked background and/or positive selection across a stable genomic landscape. Several low divergence balanced loci were also identified, with one notable locus housing numerous chemosensory receptor genes, which play a crucial role in mediating reproductive and feeding behaviours in sea snakes. This thesis provides novel insights into the demographic and genetic factors that have facilitated the terrestrial-to-marine transition in elapid snakes, and the rapid radiation in Hydrophis snakes. This work has generated numerous high-quality genomic resources, including whole genome sequencing and chromosome-scale reference genomes, that will prove to be powerful resources for future studies investigating these diverse organisms.

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School of Biological Sciences

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Thesis (Ph.D.) -- University of Adelaide, School of Biological Sciences, 2023

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This electronic version is made publicly available by the University of Adelaide in accordance with its open access policy for student theses. Copyright in this thesis remains with the author. This thesis may incorporate third party material which has been used by the author pursuant to Fair Dealing exceptions. If you are the owner of any included third party copyright material you wish to be removed from this electronic version, please complete the take down form located at: http://www.adelaide.edu.au/legals

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