The genome of Shaw’s sea snake (Hydrophis curtus) reveals secondary adaptation to its marine environment

Abstract

The transition of terrestrial snakes to marine life approximately 10 million years ago (Ma) is ideal for exploring adaptive evolution. Sea snakes possess phenotype specializations including laterally compressed bodies, paddle-shaped tails, valvular nostrils, cutaneous respiration, elongated lungs and salt glands yet knowledge on the genetic underpinnings of the transition remain limited. Herein, we report the first genome of Shaw’s sea snake (Hydrophis curtus) and use it to investigate sea snake secondary marine adaptation. A hybrid assembly strategy obtains a high quality genome. Gene family analyses date a pulsed coding-gene expansion to about 20 Ma, and these genes associate strongly with adaptations to marine environments. Analyses of selection pressure and convergent evolution discover the rapid evolution of protein-coding genes, and some convergent features. Additionally, 108 conserved non-coding elements appear to have evolved quickly, and these may underpin the phenotypic changes. Transposon elements may contribute to adaptive specializations by inserting into genomic regions around functionally related coding genes. The integration of genomic and transcriptomic analyses indicates independent origins and different components in sea snake and terrestrial snake venom; the venom gland of the sea snake harbours the highest PLA2 (17.23%) expression in selected elapids and these genes may organize tandemly in the genome. These analyses provide insights into the genetic mechanisms that underlay the secondary adaptation to marine and venom production of this sea snake.

A brief review on the natural history, venomics and the medical importance of bushmaster (Lachesis) pit viper snakes

“…Mapping the pattern of present-day venom variability into a phylogenetic and biogeographic framework may lay the foundation for understanding the evolutionary trends that have shaped the venomic landscape across the clade. In addition, the genome also encodes traces from both functionally-failed recombinations and those that passed the natural selection filter and contributed to the functional genome of the species ( Kvon et al, 2016 ; Li et al, 2018 ; Lind et al, 2019 ; Pasquesi et al, 2018 ; Peng et al, 2020 ; Perry et al, 2018 ; Reyes-Velasco et al, 2020 ; Schield et al, 2019 ). The development of comparative genomics in the last 20 years has taught us that no lineage can be studied genomically in isolation from related lineages.…”

“…Squamates exhibit some of the most extreme and fascinating biological adaptations among vertebrates ( Shaney et al, 2014 ). However, genomic resources are currently only available for a handful of squamous reptiles ( Alföldi et al, 2011 ; Castoe et al, 2013 ; Giorgianni et al, 2020 ; Green et al, 2014 ; Kerkkamp et al, 2016 ; Li et al, 2018 ; Lind et al, 2019 ; Peng et al, 2020 ; Schield et al, 2019 ; Shibata et al, 2018 ; Suryamohan et al, 2020 ; Tollis et al, 2014 ; Ullate-Agote et al, 2014 ; Vonk et al, 2013 ; Yin et al, 2016 ). Comparative Squamata omics (genomics, transcriptomics, and proteomics) will play a fundamental role in filling this gap and addressing the connection between genome evolution and the present-day adaptive phenotype for fitness related traits ( Cenik et al, 2015 ; Drukewitz and von Reumont, 2019 ; Eckalbar et al, 2013 ; Hajirasouliha and Tilgner, 2019 ).…”

The mitochondrial genome of the Hydrophis curtus (Squamata: Elapidae)

“…Shaw's sea snake (Hydrophis curtus) is a viviparous species, belongs to the genus Hydrophis and possess several morphological adaptations that associate with their marine life, such as laterally compressed bodies, paddle-shaped tails and reduced ventral scales. A genomic research of Hydrophis curtus reveal the genetic mechanism of its marine adaptation (Peng et al 2020). In our study, we obtained the mitochondrial sequence of Shaw's sea-snake based on the published genome (Peng et al 2020).…”

“…A genomic research of Hydrophis curtus reveal the genetic mechanism of its marine adaptation (Peng et al 2020). In our study, we obtained the mitochondrial sequence of Shaw's sea-snake based on the published genome (Peng et al 2020).…”

“…The Hydrophis curtus specimen was donated by the local fishermen from the coastal of Haikou, Hainan Province, China, and its DNA was stored in the Herpetological Museum of the Chengdu Institute of Biology, Chinese Academy of Sciences with the number 2160722004. The mitochondrial genome was generated from the raw data of Hydrophis curtus genome (PRJNA597425, library SRR10861676 was used) (Peng et al 2020). To annotate the mitochondrial DNA sequence, a mitochondrial genome annotation web server (MITOS) was used to predicted the gene structure and then correct the mitogenomic structure manually (Bernt et al 2013).…”