Skip to main content
bioRxiv
  • Home
  • About
  • Submit
  • ALERTS / RSS
Advanced Search
New Results

Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life historie

View ORCID ProfileBlair P. Bentley, Tomás Carrasco-Valenzuela, Elisa K. S. Ramos, Harvinder Pawar, Larissa Souza Arantes, Alana Alexander, View ORCID ProfileShreya M. Banerjee, Patrick Masterson, Martin Kuhlwilm, View ORCID ProfileMartin Pippel, Jacquelyn Mountcastle, View ORCID ProfileBettina Haase, Marcela Uliano Silva, View ORCID ProfileGiulio Formenti, View ORCID ProfileKerstin Howe, William Chow, Alan Tracey, Yumi Sims, Sarah Pelan, Jonathan Wood, View ORCID ProfileJustin R. Perrault, Kelly Stewart, View ORCID ProfileScott R. Benson, Yaniv Levy, View ORCID ProfileErica V. Todd, H. Bradley Shaffer, Peter Scott, Brian T. Henen, Robert W. Murphy, David W. Mohr, Alan F. Scott, Neil J. Gemmell, View ORCID ProfileAlexander Suh, Sylke Winkler, Françoise Thibaud-Nissen, Mariana F. Nery, Tomas Marques-Bonet, Agostinho Antunes, Yaron Tikochinski, Peter H. Dutton, View ORCID ProfileOlivier Fedrigo, Eugene W. Myers, Erich D. Jarvis, Camila J. Mazzoni, Lisa M. Komoroske
doi: https://doi.org/10.1101/2022.01.10.475373
Blair P. Bentley
1Department of Environmental Conservation, University of Massachusetts, Amherst, MA, USA;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Blair P. Bentley
  • For correspondence: bbentley@umass.edu
Tomás Carrasco-Valenzuela
2Evolutionary Genetics Department, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
3Berlin Center for Genomics in Biodiversity Research, Berlin, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Elisa K. S. Ramos
2Evolutionary Genetics Department, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
3Berlin Center for Genomics in Biodiversity Research, Berlin, Germany
4Department of Genetics, Evolution, Microbiology and Immunology, University of Campinas, Campinas, Brazil
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Harvinder Pawar
5Institut de Biologia Evolutiva, (CSIC-Universitat Pompeu Fabra), PRBB, Doctor Aiguader 88, Barcelona, Catalonia, Spain
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Larissa Souza Arantes
2Evolutionary Genetics Department, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
3Berlin Center for Genomics in Biodiversity Research, Berlin, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alana Alexander
6Department of Anatomy, School of Biomedical Sciences, University of Otago, Dunedin, New Zealand;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Shreya M. Banerjee
1Department of Environmental Conservation, University of Massachusetts, Amherst, MA, USA;
7Department of Biology, Stanford University, Stanford CA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Shreya M. Banerjee
Patrick Masterson
8National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Martin Kuhlwilm
5Institut de Biologia Evolutiva, (CSIC-Universitat Pompeu Fabra), PRBB, Doctor Aiguader 88, Barcelona, Catalonia, Spain
9Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria
10Human Evolution and Archaeological Sciences (HEAS), University of Vienna, Austria
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Martin Pippel
11Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
12Center for Systems Biology, Dresden, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Martin Pippel
Jacquelyn Mountcastle
13Vertebrate Genome Lab, The Rockefeller University, New York, NY, USA
22Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Bettina Haase
13Vertebrate Genome Lab, The Rockefeller University, New York, NY, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Bettina Haase
Marcela Uliano Silva
2Evolutionary Genetics Department, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
3Berlin Center for Genomics in Biodiversity Research, Berlin, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Giulio Formenti
13Vertebrate Genome Lab, The Rockefeller University, New York, NY, USA
14Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Giulio Formenti
Kerstin Howe
15Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Kerstin Howe
William Chow
15Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alan Tracey
15Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yumi Sims
15Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sarah Pelan
15Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jonathan Wood
15Tree of Life, Wellcome Sanger Institute, Cambridge, CB10 1SA, UK
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Justin R. Perrault
16Loggerhead Marinelife Center, Juno Beach, FL, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Justin R. Perrault
Kelly Stewart
17Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, United States
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Scott R. Benson
18Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Moss Landing, CA, USA
19Moss Landing Marine Laboratories, Moss Landing, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Scott R. Benson
Yaniv Levy
20National Sea Rescue Centre, Israel’s Nature and Parks Authority, Mevoot Yam, Michmoret, Israel
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Erica V. Todd
21School of Life and Environmental Sciences, Deakin University, Queenscliff, VIC, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Erica V. Todd
H. Bradley Shaffer
22Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA;
23La Kretz Center for California Conservation Science, Institute of the Environment and Sustainability, University of California, Los Angeles, CA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Peter Scott
22Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA;
24Department of Life, Earth, and Environmental Sciences, West Texas A&M University, Canyon, TX, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Brian T. Henen
25Environmental Affairs, Marine Air Ground Task Force and Training Command, Marine Corps Air Ground Combat Center, Twentynine Palms CA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert W. Murphy
26Centre for Biodiversity, Royal Ontario Museum, Toronto, Ontario, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
David W. Mohr
27Genetic Resources Core Facility, McKusick-Nathans Dept of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore MD 21287, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alan F. Scott
27Genetic Resources Core Facility, McKusick-Nathans Dept of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore MD 21287, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Neil J. Gemmell
28Allan Wilson Centre, Department of Anatomy, University of Otago, Dunedin, New Zealand
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alexander Suh
29School of Biological Sciences, University of East Anglia, Norwich NR4 7TU, UK
30Department of Organismal Biology, Evolutionary Biology Centre (EBC), Science for Life Laboratory, Uppsala University, Uppsala, Sweden
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Alexander Suh
Sylke Winkler
11Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
31DRESDEN concept Genome Center, Dresden, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Françoise Thibaud-Nissen
8National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Mariana F. Nery
4Department of Genetics, Evolution, Microbiology and Immunology, University of Campinas, Campinas, Brazil
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tomas Marques-Bonet
5Institut de Biologia Evolutiva, (CSIC-Universitat Pompeu Fabra), PRBB, Doctor Aiguader 88, Barcelona, Catalonia, Spain
32CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain
33Institucio Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Catalonia 08010, Spain
34Institut Català de Paleontologia Miquel Crusafont, Universitat Autonoma de Barcelona
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Agostinho Antunes
35CIIMAR/CIMAR, Centro Interdisciplinar de Investigaçãao Marinha e Ambiental, Universidade do Porto, Av. General Norton de Matos, s/n, 4450-208, Porto, Portugal
36Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, s/n, 4169-007, Porto, Portugal
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yaron Tikochinski
37Faculty of Marine Sciences, Ruppin Academic Center, Michmoret, Israel
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Peter H. Dutton
17Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, United States
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Olivier Fedrigo
13Vertebrate Genome Lab, The Rockefeller University, New York, NY, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Olivier Fedrigo
Eugene W. Myers
11Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
12Center for Systems Biology, Dresden, Germany
38Faculty of Computer Science, Technical University Dresden, Dresden, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Erich D. Jarvis
13Vertebrate Genome Lab, The Rockefeller University, New York, NY, USA
14Laboratory of Neurogenetics of Language, The Rockefeller University, New York, NY, USA
39Howard Hughes Medical Institute, Chevy Chase, MD, USA.
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Camila J. Mazzoni
2Evolutionary Genetics Department, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
3Berlin Center for Genomics in Biodiversity Research, Berlin, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lisa M. Komoroske
1Department of Environmental Conservation, University of Massachusetts, Amherst, MA, USA;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Abstract
  • Full Text
  • Info/History
  • Metrics
  • Supplementary material
  • Data/Code
  • Preview PDF
Loading

Abstract

Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 MYA, yet the genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remain largely unknown. Additionally, many populations have declined drastically 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 green (Chelonia mydas) and leatherback (Dermochelys coriacea) turtles, representing the two extant sea turtle families (MRCA ∼60 MYA). These genomes are highly syntenic and homologous, but localized non-collinearity was associated with higher copy numbers of immune, zinc-finger, or olfactory receptor (OR) genes in green turtles, and ORs related to waterborne odorants were greatly expanded in green turtles. These 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 and extremely low diversity compared to other reptiles, and a higher proportion of deleterious variants, 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.

Statement of significance Sea turtles represent a clade whose populations have undergone recent global declines. We analyzed de novo genomes for both extant sea turtle families through the Vertebrate Genomes Project to inform their conservation and evolutionary biology. The highly conserved genomes were largely differentiated by localized gene-rich regions of divergence, particularly in microchromosomes, suggesting that these overlooked genomic elements may play key functional roles in sea turtle evolution. We further demonstrate that dissimilar evolutionary histories impact standing genomic diversity and genetic load, and are critical to consider when using these metrics to assess adaptive potential and extinction risk. Examination of these relationships may be important to reveal drivers of adaptation and diversity in sea turtles and other vertebrates with conserved genome synteny.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Updated manuscript and supplementary information uploaded after the identification of some errors.

  • https://vgp.github.io/genomeark/Dermochelys_coriacea/

  • https://vgp.github.io/genomeark/Chelonia_mydas/

  • https://www.ncbi.nlm.nih.gov/assembly/GCF_009764565.3

  • https://www.ncbi.nlm.nih.gov/assembly/GCF_015237465.2

  • Abbreviations

    TE
    transposable element
    RE
    repetitive element
    RRC
    region of reduced collinearity
    FP
    Fibropapillomatosis
    ROH
    runs of homozygosity
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
    Back to top
    PreviousNext
    Posted January 18, 2022.
    Download PDF

    Supplementary Material

    Data/Code
    Email

    Thank you for your interest in spreading the word about bioRxiv.

    NOTE: Your email address is requested solely to identify you as the sender of this article.

    Enter multiple addresses on separate lines or separate them with commas.
    Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life historie
    (Your Name) has forwarded a page to you from bioRxiv
    (Your Name) thought you would like to see this page from the bioRxiv website.
    CAPTCHA
    This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
    Share
    Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life historie
    Blair P. Bentley, Tomás Carrasco-Valenzuela, Elisa K. S. Ramos, Harvinder Pawar, Larissa Souza Arantes, Alana Alexander, Shreya M. Banerjee, Patrick Masterson, Martin Kuhlwilm, Martin Pippel, Jacquelyn Mountcastle, Bettina Haase, Marcela Uliano Silva, Giulio Formenti, Kerstin Howe, William Chow, Alan Tracey, Yumi Sims, Sarah Pelan, Jonathan Wood, Justin R. Perrault, Kelly Stewart, Scott R. Benson, Yaniv Levy, Erica V. Todd, H. Bradley Shaffer, Peter Scott, Brian T. Henen, Robert W. Murphy, David W. Mohr, Alan F. Scott, 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 W. Myers, Erich D. Jarvis, Camila J. Mazzoni, Lisa M. Komoroske
    bioRxiv 2022.01.10.475373; doi: https://doi.org/10.1101/2022.01.10.475373
    Reddit logo Twitter logo Facebook logo LinkedIn logo Mendeley logo
    Citation Tools
    Differential sensory and immune gene evolution in sea turtles with contrasting demographic and life historie
    Blair P. Bentley, Tomás Carrasco-Valenzuela, Elisa K. S. Ramos, Harvinder Pawar, Larissa Souza Arantes, Alana Alexander, Shreya M. Banerjee, Patrick Masterson, Martin Kuhlwilm, Martin Pippel, Jacquelyn Mountcastle, Bettina Haase, Marcela Uliano Silva, Giulio Formenti, Kerstin Howe, William Chow, Alan Tracey, Yumi Sims, Sarah Pelan, Jonathan Wood, Justin R. Perrault, Kelly Stewart, Scott R. Benson, Yaniv Levy, Erica V. Todd, H. Bradley Shaffer, Peter Scott, Brian T. Henen, Robert W. Murphy, David W. Mohr, Alan F. Scott, 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 W. Myers, Erich D. Jarvis, Camila J. Mazzoni, Lisa M. Komoroske
    bioRxiv 2022.01.10.475373; doi: https://doi.org/10.1101/2022.01.10.475373

    Citation Manager Formats

    • BibTeX
    • Bookends
    • EasyBib
    • EndNote (tagged)
    • EndNote 8 (xml)
    • Medlars
    • Mendeley
    • Papers
    • RefWorks Tagged
    • Ref Manager
    • RIS
    • Zotero
    • Tweet Widget
    • Facebook Like
    • Google Plus One

    Subject Area

    • Genomics
    Subject Areas
    All Articles
    • Animal Behavior and Cognition (4230)
    • Biochemistry (9123)
    • Bioengineering (6766)
    • Bioinformatics (23968)
    • Biophysics (12109)
    • Cancer Biology (9510)
    • Cell Biology (13753)
    • Clinical Trials (138)
    • Developmental Biology (7623)
    • Ecology (11674)
    • Epidemiology (2066)
    • Evolutionary Biology (15492)
    • Genetics (10631)
    • Genomics (14310)
    • Immunology (9473)
    • Microbiology (22822)
    • Molecular Biology (9086)
    • Neuroscience (48919)
    • Paleontology (355)
    • Pathology (1480)
    • Pharmacology and Toxicology (2566)
    • Physiology (3840)
    • Plant Biology (8322)
    • Scientific Communication and Education (1468)
    • Synthetic Biology (2295)
    • Systems Biology (6180)
    • Zoology (1299)