Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

Blair P Bentley, Tomas Carrasco-Valenzuela, Elisa Karen da Silva Ramos, Harvinder Pawar, Larissa Souza Arantes, Alana Alexander, Shreya Banerjee, Patrick Masterson, Martin Kuhlwilm, Martin Pippel, Jacquelyn Mountcastle, Bettina Haase, Marcela Uliano-Silva, Giulio Formenti, Kerstin Howe, William Chow, Alan Tracey, Ying Sims, Sarah Pelan, Jonathan WoodKelsey Yetsko, Justin Perrault, Kelly Stewart, Scott R. Benson, Yaniv Levy, Erica Todd, Howard Bradley Shaffer, Peter Scott, Brian Henen, Robert W. Murphy, David Mohr, Alan F. Scott, David Duffy, Neil J. Gemmell, Alexander Suh, Sylke Winkler, Françoise Thibaud-Nissen, Mariana F. Nery, Tomas Marques-Bonet, Agostinho Antunes, Yaron Tikochinski, Peter H. Dutton, Olivier Fedrigo, Eugene Myers, Erich Jarvis, Camila Mazzoni, Lisa M. Komoroske

Publications: Contribution to journalArticlePeer Reviewed

Abstract

Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 Mya. The genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remains largely unknown. Additionally, many populations have drastically declined due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for the leatherback (Dermochelys coriacea) and green (Chelonia mydas) turtles, representing the two extant sea turtle families. These genomes are highly syntenic and homologous, but localized regions of noncollinearity were associated with higher copy numbers of immune, zinc-finger, and olfactory receptor (OR) genes in green turtles, with ORs related to waterborne odorants greatly expanded in green turtles. Our findings suggest that divergent evolution of these key gene families may underlie immunological and sensory adaptations assisting navigation, occupancy of neritic versus pelagic environments, and diet specialization. Reduced collinearity was especially prevalent in microchromosomes, with greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, diversity and demographic histories starkly contrasted between species, indicating that leatherback turtles have had a low yet stable effective population size, exhibit extremely low diversity compared with other reptiles, and harbor a higher genetic load compared with green turtles, reinforcing concern over their persistence under future climate scenarios. These genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.

Original languageEnglish
Article numbere2201076120
JournalProceedings of the National Academy of Sciences
Volume120
Issue number7
DOIs
Publication statusPublished - 14 Feb 2023

Austrian Fields of Science 2012

  • 106054 Zoology

Keywords

  • conservation genomics
  • demographic history
  • gene evolution
  • genetic diversity
  • marine turtle

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