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Ancient mitogenomics elucidates diversity of extinct West Indian tortoises

  • 1.

    TTWG [Turtle Taxonomy Working Group; Rhodin, A. G. J. et al.] Turtles of the World. Annotated Checklist and Atlas of Taxonomy, Synonymy, Distribution, and Conservation Status (8th Ed.) (Chelonian Research Foundation and Turtle Conservancy, Chelonian Research Monographs 7, 2017).

  • 2.

    TEWG [Turtle Extinctions Working Group; Rhodin, A. G. J. et al.] Turtles and Tortoises of the World During the Rise and Global Spread of Humanity: First Checklist and Review of Extinct Pleistocene and Holocene Chelonians (IUCN/SSC Tortoise and Freshwater Turtle Specialist Group, Chelonian Research Monographs 5, 2015).

  • 3.

    Clausen, C. J., Cohen, A. D., Emiliani, C., Holman, J. A. & Stipp, J. J. Little Salt Spring, Florida: A unique underwater site. Science 203, 609–614 (1979).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 4.

    Holman, J. A. & Clausen, C. J. Fossil vertebrates associated with Paleo-Indian artifact at Little Salt Spring, Florida. J. Vertebr. Paleontol. 4, 146–154 (1984).

    Article  Google Scholar 

  • 5.

    Cantalamessa, G. et al. A new vertebrate fossiliferous site from the Late Quaternary at San José on the north coast of Ecuador: Preliminary note. J. South Am. Earth Sci. 14, 331–334 (2001).

    ADS  Article  Google Scholar 

  • 6.

    Aguilera Socorro, O. Tesoros paleontológicos de Venezuela. El Cuaternario del Estado Falcón (Ministerio de la Cultura, Instituto del Patrimonio Cultural, Caracas, 2006).

    Google Scholar 

  • 7.

    Zacarías, G. G., de la Fuente, M. S., Fernández, M. S. & Zurita, A. E. Nueva especie de tortuga terrestre gigante del género Chelonoidis Fitzinger, 1835 (Cryptodira: Testudinidae), del miembro inferior de la Formación Toropí/Yupoí (Pleistoceno tardío/Lujanense), Bella Vista, Corrientes, Argentina. Ameghiniana 50, 298–318 (2013).

    Article  Google Scholar 

  • 8.

    Zacarías, G. G., de la Fuente, M. S. & Zurita, A. E. Testudinoidea Fitzinger (Testudines: Cryptodira) de la Formación Toropí/Yupoí (ca. 58–28 ka) en la Provincia de Corrientes, Argentina: Taxonomía y aspectos paleoambientales. Rev. Bras. Paleontol. 17, 389–404 (2014).

    Article  Google Scholar 

  • 9.

    Torres Chiriboga, F. J. Histología ósea de una tortuga gigante del Pleistoceno (Testudinidae) de Ecuador continental, con comentarios del origen de las tortugas de Galápagos (Disertación previa, Pontificia Universidad Católica del Ecuador, Quito, 2016).

    Google Scholar 

  • 10.

    Cadena, E. A. & Román-Carrión, J. L. A review of the fossil record of Ecuador, with insights about its challenges and future development. Ameghiniana 55, 571–591 (2018).

    Article  Google Scholar 

  • 11.

    Franz, R., Albury, N. A. & Steadman, D. W. Extinct tortoises from the Turks and Caicos Islands. Florida Mus. Nat. Hist. Bull. 58, 1–38 (2020).

    Google Scholar 

  • 12.

    Williams, E. E. Testudo cubensis and the evolution of Western Hemisphere tortoises. Bull. Am. Mus. Nat. Hist. 95, 1–36 (1950).

    Google Scholar 

  • 13.

    Williams, E. E. A new fossil tortoise from Mona Island, West Indies, and a tentative arrangement of the tortoises of the world. Bull. Am. Mus. Nat. Hist. 99, 545–560 (1952).

    Google Scholar 

  • 14.

    Auffenberg, W. Notes on West Indian tortoises. Herpetologica 23, 34–44 (1967).

    Google Scholar 

  • 15.

    Franz, R. & Woods, C. A. A fossil tortoise from Hispaniola. J. Herpetol. 17, 79–81 (1983).

    Article  Google Scholar 

  • 16.

    Franz, R. & Franz, S. A new fossil land tortoise in the genus Chelonoidis (Testudines: Testudinidae) from the northern Bahamas, with an osteological assessment of other Neotropical tortoises. Florida Mus. Nat. Hist. Bull. 49, 1–44 (2009).

    Google Scholar 

  • 17.

    Steadman, D. W. et al. Exceptionally well preserved late Quaternary plant and vertebrate fossils from a blue hole on Abaco, The Bahamas. Proc. Natl. Acad. Sci. USA 104, 19897–19902 (2007).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 18.

    Hastings, A. K., Krigbaum, J., Steadman, D. W. & Albury, N. A. Domination by reptiles in a terrestrial food web of the Bahamas prior to human occupation. J. Herpetol. 48, 380–388 (2014).

    Article  Google Scholar 

  • 19.

    Kehlmaier, C. et al. Tropical ancient DNA reveals relationships of the extinct Bahamian giant tortoise Chelonoidis alburyorum. Proc. R. Soc. B 284, 20162235 (2017).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 20.

    Steadman, D. W. et al. The paleoecology and extinction of endemic tortoises in the Bahamian Archipelago. Holocene 30, 420–427 (2020).

    ADS  Article  Google Scholar 

  • 21.

    Albury, N. A., Franz, R., Rimoli, P., Lehman, P. & Rosenberger, A. L. Fossil land tortoises (Testudines: Testudinidae) from the Dominican Republic, West Indies, with a description of a new species. Am. Mus. Novit. 3904, 1–28 (2018).

    Article  Google Scholar 

  • 22.

    Fulton, T. L. & Shapiro, B. Setting up an ancient DNA laboratory. In Ancient DNA: Methods and Protocols. Methods in Molecular Biology, Vol. 1963 (eds Shapiro, B. et al.), 1–13 (Humana Press, Totowa, 2019).

    Google Scholar 

  • 23.

    Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. USA 110, 15758–15763 (2013).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 24.

    Gansauge, M.-T. & Meyer, M. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat. Protoc. 8, 737–748 (2013).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 25.

    Korlević, P. et al. Reducing microbial and human contamination in DNA extractions from ancient bones and teeth. Biotechniques 58, 87–93 (2015).

    Google Scholar 

  • 26.

    Maricic, T., Whitten, M. & Pääbo, S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One 5, e14004 (2010).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 27.

    Horn, S. Target enrichment via DNA hybridization capture. In Ancient DNA: Methods and Protocols. Methods in Molecular Biology, Vol. 840 (eds Shapiro, B. & Hofreiter, M.), 177–188 (Springer, Berlin, 2012).

    Google Scholar 

  • 28.

    Jiang, H., Lei, R., Ding, S. W. & Zhu, S. Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinform. 15, 182 (2014).

    Article  Google Scholar 

  • 29.

    Bushnell, B., Rood, J. & Singer, E. BBMerge—accurate paired shotgun read merging via overlap. PLoS One 12, e0185056 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 30.

    Wingett, S. W. & Andrews, S. FastQ Screen: A tool for multi-genome mapping and quality control [version 2; referees: 4 approved]. F1000Research 7, 1338 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    Hahn, C., Bachmann, L. & Chevreux, B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res. 41, 1–9 (2013).

    Article  CAS  Google Scholar 

  • 32.

    Milne, I. et al. Using Tablet for visual exploration of second-generation sequencing data. Brief. Bioinform. 14, 193–202 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 33.

    Quinlan, A. R. & Hall, I. M. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 34.

    Kehlmaier, C. et al. Ancient mitogenomics clarifies radiation of extinct Mascarene giant tortoises. Sci. Rep. 9, 17487 (2019).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 35.

    Poulakakis, N. et al. Colonization history of Galapagos giant tortoises: Insights from mitogenomes support the progression rule. J. Zool. Syst. Evol. Res. 58, 1262–1275 (2020).

    Article  Google Scholar 

  • 36.

    Thompson, J. D., Higgins, D. G. & Gibson, T. J. Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 37.

    Hall, T. A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98 (1999).

    CAS  Google Scholar 

  • 38.

    Bernt, M. et al. MITOS: Improved de novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol. 69, 313–319 (2013).

    PubMed  Article  Google Scholar 

  • 39.

    Kumar, S., Stecher, G., Knyaz, C. & Tamura, K. MEGA X: Molecular Evolutionary Genetic Analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 41.

    Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 42.

    Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2016).

    Google Scholar 

  • 43.

    Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 5, 901–904 (2018).

    Article  CAS  Google Scholar 

  • 44.

    Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 45.

    Woods, R. et al. Rapid size change associated with intra-island evolutionary radiation in extinct Caribbean “island shrews”. BMC Evol. Biol. 29, 106 (2020).

    Article  CAS  Google Scholar 

  • 46.

    Geist, D., Snell, H. L., Snell, H. M., Goddard, C. & Kurz, M. Paleogeography of the Galápagos Islands and biogeographical implications. In The Galápagos: A Natural Laboratory for the Earth Sciences, Vol. 204 (eds Harpp, K., Mittelstaedt, E., d’Ozouville, N. & Graham, D.) 145–166 (American Geophysical Union, New York, 2014).

    Google Scholar 

  • 47.

    Hearty, P. J., Kindler, P., Cheng, H. & Edwards, R. A +20 m middle Pleistocene sea-level highstand (Bermuda and the Bahamas) due to partial collapse of Antarctic ice. Geology 27, 375–378 (1999).

    ADS  Article  Google Scholar 

  • 48.

    Bowen, D. Sea level 400 000 years ago (MIS 11): Analogue for present and future sea-level? Clim. Past 6, 19–29 (2010).

    Article  Google Scholar 

  • 49.

    Steadman, D. W. & Franklin, J. Origin, paleoecology, and extirpation of bluebirds and crossbills in the Bahamas across the last glacial-interglacial transition. Proc. Natl. Acad. Sci. USA 114, 9924–9929 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 50.

    Fritz, U., Široký, P., Kami, H. & Wink, M. Environmentally caused dwarfism or a valid species—Is Testudo weissingeri Bour, 1996 a distinct evolutionary lineage? New evidence from mitochondrial and nuclear genomic markers. Mol. Phylogenet. Evol. 37, 389–401 (2005).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 51.

    Fritz, U. et al. Phenotypic plasticity leads to incongruence between morphology-based taxonomy and genetic differentiation in western Palaearctic tortoises (Testudo graeca complex; Testudines, Testudinidae). Amphibia-Reptilia 28, 97–121 (2007).

    Article  Google Scholar 

  • 52.

    Fritz, U. et al. Mitochondrial phylogeography and subspecies of the wide-ranging sub-Saharan leopard tortoise Stigmochelys pardalis (Testudines: Testudinidae)—a case study for the pitfalls of pseudogenes and GenBank sequences. J. Zool. Syst. Evol. Res. 48, 348–359 (2010).

    Article  Google Scholar 

  • 53.

    Fritz, U. et al. Northern genetic richness and southern purity, but just one species in the Chelonoidis chilensis complex. Zool. Scr. 41, 220–232 (2012).

    Article  Google Scholar 

  • 54.

    Carlson, L. A. & Keegan, W. F. Resource depletion in the prehistoric northern West Indies. In Voyages of Discovery (ed. Fitzpatrick, S. M.) 85–107 (Praeger, Westport, 2004).

    Google Scholar 

  • 55.

    Keegan, W. F. Taino Indian Myth and Practice: The Arrival of the Stranger King (University Press of Florida, Gainesville, 2007).

    Google Scholar 

  • 56.

    Oswald, J. A. et al. Ancient DNA and high-resolution chronometry reveal a long-term human role in the historical diversity and biogeography of the Bahamian hutia. Sci. Rep. 10, 1373 (2020).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 57.

    Loire, E. & Galtier, N. Lacking conservation genomics in the giant Galápagos tortoise. bioRxiv 101980, 1–14 (2017).

    Google Scholar 

  • 58.

    Fontaine, M. C. A genomic perspective is needed for the re-evaluation of species boundaries, evolutionary trajectories, and conservation strategies of the Galápagos giant tortoises. PCI Evol. Biol. 100031, 1–3 (2017).

    Google Scholar 

  • 59.

    Vargas-Ramírez, M., Maran, J. & Fritz, U. Red- and yellow-footed tortoises (Chelonoidis carbonaria, C. denticulata) in South American savannahs and forests: Do their phylogeographies reflect distinct habitats? Org. Divers. Evol. 10, 161–172 (2010).

    Article  Google Scholar 

  • 60.

    Blake, S. et al. Seed dispersal by Galápagos tortoises. J. Biogeogr. 39, 1961–1972 (2012).

    Article  Google Scholar 

  • 61.

    Walton, R. et al. In the land of giants: Habitat use and selection of the Aldabra giant tortoise on Aldabra Atoll. Biodiv. Conserv. 28, 3183–3198 (2019).

    Article  Google Scholar 


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