New insights into the origin of the Galápagos tortoises with a tip-dated analysis of Testudinidae

LITERATURE CITED

• Arbogast, B. S., Drovetski, S. V., Curry, R. L., Boag, P. T., Seutin, G., Grant, P. R., Grant, B. R., & Anderson, D. J. (2006). The origin and diversification of Galápagos mockingbirds. Evolution, 60(2), 370–382. doi:10.1111/j.0014-3820.2006.tb01113
   PubMed Web of Science ®Google Scholar
• Arcila, D., Pyron, R. A., Tyler, J. C., Ortí, G., & Betancur-R, R. (2015). An evaluation of fossil tip-dating versus node-age calibrations in tetraodontiform fishes (Teleostei: Percomorphaceae). Molecular Phylogenetics and Evolution, 82, 131–145. https://doi.org/10.1016/j.ympev.2014.10.011
   PubMed Web of Science ®Google Scholar
• Arnold, E. N. (1979). Indian Ocean giant tortoises: their systematics and island adaptations. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 286(1011), 127–145. doi:10.1098/rstb.1979.0022
   Web of Science ®Google Scholar
• Auffenberg, W. (1971). A new fossil tortoise, with remarks on the origin of South American Testudinines. Copeia, 1971, 106–117. doi:10.2307/1441604
   Google Scholar
• Baur, G. (1890). Galápagos islands. Proceedings of the American Antiquarian Society, 7, 418–423.
   Google Scholar
• Batsch, A. J. G. K. (1788). Versuch einer anleitung, zur kenntniß und geschichte der thiere und mineralien. Akademische Buchhandlung.
   Google Scholar
• Bell, C. J., Gauthier, J. A., & Bever, G. S. (2010). Covert biases, circularity, and apomorphies: a critical look at the North American Herpetofaunal Stability Hypothesis. Quaternary International, 217, 30–36. https://doi.org/10.1016/j.quaint.2009.08.009
   Web of Science ®Google Scholar
• Bever, G. S. (2005). Variation in the ilium of North American Bufo (Lissamphibia; Anura) and its implications for species-level identification of fragmentary anuran fossils. Journal of Vertebrate Paleontology, 25(3), 548–560. https://doi.org/10.1671/0272-4634(2005)025[0548:VITION]2.0.CO;2
   Web of Science ®Google Scholar
• Bojanus, L. H. (1819–1821) (reprinted 1970). Anatome testudinis Europaeae. Society for the Study of Amphibians and Reptiles.
   Google Scholar
• Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie, H. A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., … & Drummond, A. J. (2019). BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650
   PubMed Web of Science ®Google Scholar
• Caccone, A., Gibbs, J. P., Ketmaier, V., Suatoni, E., & Powell, J. R. (1999). Origin and evolutionary relationships of giant Galápagos tortoises. Proceedings of the National Academy of Science, 96(23), 13223–13228. doi:10.1073/pnas.96.23.13223
   PubMed Web of Science ®Google Scholar
• Cadena, E. A., Anaya, F., & Croft, D. (2015). Giant fossil tortoise and freshwater chelid turtle remains from the middle Miocene, Quebrada Honda, Bolivia: evidence for lower paleoelevations for the southern Altiplano. Journal of South American Earth Sciences, 64, 190–198. https://doi.org/10.1016/j.jsames.2015.10.013
   Web of Science ®Google Scholar
• Cadena, E. A., Bourque, J., Rincon, A., Bloch, J., Jaramillo, C., & MacFadden, B. (2012). New turtles (Chelonia) from the late Eocene through late Miocene of the Panama Canal Basin. Journal of Paleontology, 86(3), 539–557. https://doi.org/10.1666/11-106.1
   Web of Science ®Google Scholar
• Cadena, E. A. & Jaramillo, C. (2015). Early to middle Miocene turtles from the northernmost tip of South America; giant tortoises, chelids, and podocnemidids from the Castilletes Formation, Colombia. Ameghiniana, 52(2), 188–203. http://doi.org/10.5710/AMGH.10.11.2014.2835
   Web of Science ®Google Scholar
• Cantalamessa, G., Di Celma, C., Bianucci, G., Carnevale, G., Coltorti, M., Delfino, M., Ficcarelli, G., Moreno Espinosa, M., Naldini, D., Pieruccini, P., Ragaini, l., Rook, L., Rossi, M., Tito, G., Torre, D., & Landini, W. (2001). A new vertebrate fossiliferous site from the Late Quaternary at San José on the north coast of Ecuador: preliminary note. Journal of South American Earth Sciences, 14(3), 331–334. https://doi.org/10.1016/S0895-9811(01)00027-X
   Web of Science ®Google Scholar
• Carranza, S., Arnold, E. N., Mateo, J. A., & López-Jurado, L. F. (2001). Parallel gigantism and complex colonization patterns in the Cape Verde scincid lizards Mabuya and Macroscincus (Reptilia: Scincidae) revealed by mitochondrial DNA sequences. Proceedings of the Royal Society B: Biological Sciences, 268(1476), 1595–1603. doi:10.1098/rspb.2001.1699
   PubMed Web of Science ®Google Scholar
• Carrillo-Briceño, J. D., Aguilera, O. A., Benites-Palomino, A., Hsiou, A. S., Birindelli, J. L. O., Adnet, S., Cadena, E. A., & Scheyer, T. M. (2021). A historical vertebrate collection from the Middle Miocene of the Peruvian Amazon. Swiss Journal of Palaeontology. 140(1), 26. doi:10.1186/s13358-021-00239-7
   Web of Science ®Google Scholar
• Crouch, N. M. A., & Clarke, J. A. (2019). Body size evolution in palaeognath birds is consistent with Neogene cooling-linked gigantism. Palaeogeography Palaeoclimatology Palaeoecology, 532, 109224. doi:10.1016/j.palaeo.2019.05.046
   Web of Science ®Google Scholar
• de la Fuente, M. S. (1994). Descripción de nuevos especímenes y relaciones filogenéticas de Chelonoidis gringorum (Simpson, 1942) (Chelonii: Testudinidae) del Mioceno temprano de Patagonia Central, Argentina. Studia Geologica Salmanticensia, 30, 107–131.
   Google Scholar
• de la Fuente, M. S., Sterli, J., & Maniel, I. (2014). Origin, evolution and biogeographic history of South American turtles. Springer Earth System Sciences. doi:10.1007/978-3-319-00518-8
   Google Scholar
• de la Fuente, M. S., Zacarías, G. G., & Vlachos, E. (2018). A review of the fossil record of South American turtles of the clade Testudinoidea. Bulletin of the Peabody Museum of Natural History, 59(2), 269–286. doi:10.3374/014.059.0201
   Web of Science ®Google Scholar
• Deza A., Cadena E. A., and Martinez, J-N. (2019). Pleistocene Fossil Turtles (Testudinoidea, Cryptodira) from the Talara Tar Seeps, Peru. Revista Peruana de Biología. 26(2), 189–200. doi: http://doi.org/10.15381/rpb.v26i2.15118
   Google Scholar
• Edmund, A.G. (1965). A Late Pleistocene fauna from the Santa Elena Peninsula, Ecuador. Life Sciences Contribution, Royal Ontario Museum, 63, 1–21.
   Google Scholar
• Ficcarelli, G., Coltorti, M., Moreno-Espinosa, M., Pieruccini, P. L., Rook, L., & Torre, D. (2003). A model for the Holocene extinction of the mammal megafauna in Ecuador. Journal of South American Earth Sciences, 15(8), 835–845. doi:10.1016/S0895-9811(02)00145-1
   Web of Science ®Google Scholar
• Fitzinger, L. J. (1836). Entwurf einer systematischen Anordnung der Schildkröten. Annales des Wiener Museums der Naturgeschichte, 1, 105–128.
   Google Scholar
• Franz, R., & Franz, S. E. (2009). A new fossil land tortoise in the genus Chelonoidis (Testudines: Testudinidae) from the northern Bahamas: with an osteological assessment of other neotropical tortoises. Bulletin of the Florida Museum of Natural History, 49(1), 1–44.
   Google Scholar
• Goloboff, P. A., Farris, J., & Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786. https://doi.org/10.1111/j.1096-0031.2008.00217.x
   Web of Science ®Google Scholar
• Gunther, A. C. L. G. (1875). Description of the living and extinct races of gigantic land-tortoises.—parts I. & II. Introduction, and the tortoises of the Galápagos islands. Philosophical Transactions of the Royal Society of London, 165, 251–284. doi:10.1098/rspl.1873.0079
   Google Scholar
• Hawlitschek, O., Toussaint, E. F. A., Gehring, P. S., Ratsoavina, F. M., Cole, N., Crottini, A., Nopper, J., Lam, A. W., Vences, M., & Glaw, F. (2017). Gecko phylogeography in the Western Indian Ocean region: the oldest clade of Ebenavia inunguis lives on the youngest island. Journal of Biogeography, 44(2), 409–420. doi:10.1111/jbi.12912
   Web of Science ®Google Scholar
• Hayes, F. E., Beaman, K. R., Hayes, W. K., & Harris Jr, L. E. (1988). Defensive behavior in the Galápagos tortoise (Geochelone elephantopus), with comments on the evolution of insular gigantism. Herpetologica, 44(1), 11–17.
   Web of Science ®Google Scholar
• Hoeck, P. E., Bollmer, J. L., Parker, P. G., & Keller, L. F. (2010). Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mockingbird populations (Mimus spp.). Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1543), 1127–1138. doi:10.1098/rstb.2009.0311
   PubMed Web of Science ®Google Scholar
• Hoffstetter, R. (1952). Les mammifères Pléistocènes de la République de l'Equateur. Mémoires, Société Géologique de France, 66, 1–391.
   Google Scholar
• Itescu, Y., Karraker, N. E., Raia, P., Pritchard, P. C. H., & Meiri, S. (2014). Is the island rule general? Turtles disagree. Global Ecology and Biogeography, 23(6), 689–700. doi:10.1111/geb.12149
   Web of Science ®Google Scholar
• Jaffe, A. L., Slater, G. J., & Alfaro, M. E. (2011). The evolution of island gigantism and body size variation in tortoises and turtles. Biology Letters, 7(4), 558–561. doi:10.1098/rsbl.2010.1084
   PubMed Web of Science ®Google Scholar
• Jensen, E. L., Gaughran, S. J., Fusco, N. A., Poulakakis, N., Tapia, W., Sevilla, C., Málaga, J., Mariani, C., Gibbs, J. P., & Caccone, A. (2022). The Galápagos giant tortoise Chelonoidis phantasticus is not extinct. Communications Biology, 5(1), 1–8. doi:10.1038/s42003-022-03483
   PubMed Web of Science ®Google Scholar
• Joos, J., Pimiento, C., Miles, D. B., & Müller, J. (2022). Quaternary megafauna extinctions altered body size distribution in tortoises. Proceedings of the Royal Society B: Biological Sciences, 289(1987), 20221947. https://doi.org/10.1098/rspb.2022.1947
   PubMed Web of Science ®Google Scholar
• Kehlmaier, C., Albury, N. A., Steadman, D. W., Graciá, E., Franz, R., & Fritz, U. (2021). Ancient mitogenomics elucidates diversity of extinct West Indian tortoises. Scientific Reports, 11(3224), 1–9. https://doi.org/10.1038/s41598-021-82299-w
   PubMed Web of Science ®Google Scholar
• Kehlmaier, C., Barlow, A., Hastings, A. K., Vamberger, M., Paijmans, J. L. A., Steadman, D. W., Albury, N. A., Franz, R., Hofreiter, M., & Fritz, U. (2017). Tropical ancient DNA reveals relationships of the extinct Bahamian giant tortoise Chelonoidis alburyorum. Proceedings of the Royal Society B: Biological Sciences, 284(1846), 20162235. doi:10.1098/rspb.2016.2235
   PubMed Web of Science ®Google Scholar
• Keogh, J. S., Scott, I. A. W., & Hayes, C. (2005). Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes. Evolution, 59(1), 226–233. doi:10.1111/j.0014-3820.2005.tb00909
   PubMed Web of Science ®Google Scholar
• Lindsey, E. L., & Lopez, E. X. (2015). Tanque Loma, a new late-Pleistocene megafaunal tar seep locality from southwest Ecuador. Journal of South American Earth Sciences, 57, 61–82. doi:10.1016/j.jsames.2014.11.003
   Web of Science ®Google Scholar
• Linnaeus, C. (1758). Systema naturae, Volume 1. Laurentius Salvius.
   Google Scholar
• Lovette, I. J., Arbogast, B. S., Curry, R. L., Zink, R. M., Botero, C. A., Sullivan, J. P., Talaba, A. L., Harris, R. B., Rubenstein, D. R., Ricklefs, R. E., & Bermingham, E. (2012). Phylogenetic relationships of the mockingbirds and thrashers (Aves: Mimidae). Molecular Phylogenetics and Evolution, 63(2), 219–229. doi:10.1016/j.ympev.2011.07.009
   PubMed Web of Science ®Google Scholar
• Lyson, T. R., Bhullar, B-A. S., Bever, G. S., Joyce, W. G., de Queiroz, K., Abzhanov, A., & Gauthier, J. A. (2013). Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell. Evolution & Development, 15(5), 317–325. DOI: 10.1111/ede.12041
   PubMed Web of Science ®Google Scholar
• Oriozabala, C., Sterli, J., & Ruiz, L. G. (2017). Morphology of the mid-sized tortoises (Testudines: Testudinidae) from the Middle Miocene of Northwestern Chubut (Argentina). Ameghiniana, 55(1), 30–54.
   Web of Science ®Google Scholar
• Paleobiology Database. (n.d.). the Paleobiology Database. Retrieved March, 8, 2023, from http://paleobiodb.org/data1.2/occs/list.csv?datainfo&rowcount&base_name=Testudinidae
   Google Scholar
• Parham, J. F., Donoghue, P. C., Bell, C. J., Calway, T. D., Head, J. J., Holroyd, P. A., Inoue, J., Irmis, R. B., Joyce, W. G., Ksepka, T. D., Patané, J. S. L., Smith, N. D., Tarver, J. E., van Tuinen, M., Yang, Z., Angielczyk, K. D., Greenwood, J. M., Hipsley, C. A., Jacobs, L., Makovicky, P. J., … Benton, M. J. (2012). Best practices for justifying fossil calibrations. Systematic Biology, 61(2), 346–359. https://doi.org/10.1093/sysbio/syr107
   PubMed Web of Science ®Google Scholar
• Pereira, A. G., Sterli, J., Moreira, F. R. R., & Schrago, C. G. (2017). Multilocus phylogeny and statistical biogeography clarify the evolutionary history of major lineages of turtles. Molecular Phylogenetics and Evolution, 113, 59–66. doi:10.1016/j.ympev.2017.05.008
   PubMed Web of Science ®Google Scholar
• Poulakakis, N., Russello, M., Geist, D., & Caccone, A. (2012). Unravelling the peculiarities of island life: vicariance, dispersal and the diversification of the extinct and extant giant Galápagos tortoises. Molecular Ecology, 21(1), 160–173. doi:10.1111/j.1365-294X.2011.05370
   PubMed Web of Science ®Google Scholar
• Pritchard, P. H. (1984). Evolution and zoogeography of South American turtles. Studia Geologica Salmanticensia, 1, 225–233.
   Google Scholar
• Pritchard, P. H. (1996). The Galápagos tortoises: nomenclatural and survival status. Chelonian Research Foundation in association with Conservation International and Chelonia Institute.
   Google Scholar
• Pyron, R. A. (2011). Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Systematic Biology, 60(4), 466–481. https://doi.org/10.1093/sysbio/syr047
   PubMed Web of Science ®Google Scholar
• Ruiz-Escobar, S. (2022a). Media 000423461: Whole Body [CTImageSeries] [CT] [Data set]. MorphoSource. https://www.morphosource.org/concern/media/000423461?locale=en
   Google Scholar
• Ruiz-Escobar, S. (2022b). Media 000423473: Whole Body [CTImageSeries] [CT] [Data set]. MorphoSource https://www.morphosource.org/concern/media/000423473?locale=en
   Google Scholar
• Sánchez, J., Holley, J. A., Poljak, S., Bolzan, A. D., & Bravi, C. M. (2017). Phylogenetic and divergence time analysis of the Chelonoidis chilensis complex (Testudines: Testudinidae). Zootaxa, 4320(3), 487–504. https://doi.org/10.11646/zootaxa.4320.3.5
   Web of Science ®Google Scholar
• Senczuk, G., García, A., Colangelo, P., Annesi, F., & Castiglia, R. (2014). Morphometric and genetic divergence in island and mainland populations of Anolis nebulosus (Squamata: Polychrotidae) from Jalisco (Mexico): an instance of insular gigantism. Italian Journal of Zoology, 81(2), 204–214. doi:10.1080/11250003.2014.911973
   Web of Science ®Google Scholar
• Simpson, G. G. (1942). A Miocene tortoise from Patagonia. American Museum Novitates, 1209, 1–6.
   Google Scholar
• Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9), 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
   PubMed Web of Science ®Google Scholar
• Sulloway, F. J. (1982). Darwin and his finches: The evolution of a legend. Journal of the History of Biology, 15, 1–53. doi:10.1007/BF00132004
   Google Scholar
• Thomson, R. C., Spinks, P. Q., & Shaffer, H. B. (2021). A global phylogeny of turtles reveals a burst of climate-associated diversification on continental margins. Proceedings of the National Academy of Science, 118(7), e2012215118. (doi:10.1073/pnas.2012215118)
   PubMed Web of Science ®Google Scholar
• Van Denburgh, J. (1914). The gigantic land tortoises of the Galápagos Archipelago. Proceedings of the California Academy of Sciences, fourth series, 2, 203–374.
   Google Scholar
• Vlachos, E., & Rabi, M. (2018). Total evidence analysis and body size evolution of extant and extinct tortoises (Testudines: Cryptodira: Pan-Testudinidae). Cladistics, 34(6), 652–683. doi:10.1111/cla.12227
   PubMed Web of Science ®Google Scholar
• von der Heydt, A., & Dijkstra, H. A. (2006). Effect of ocean gateways on the global ocean circulation in the late Oligocene and early Miocene. Paleoceanography, 21(1), PA1011. doi:10.1029/2005PA001149
   Google Scholar
• Walker, J. D., Geissman, J. W., & compilers. (2022). Geologic Time Scale v. 6.0: Geological Society of America. https://doi.org/10.1130/2022.CTS006C
   Google Scholar
• Wallace, A. R. (1881) (1998). Island Life, Prometheus.
   Google Scholar
• Wiens, J. J. (1999). Polymorphism in systematics and comparative biology. Annual Review in Ecology and Systematics, 30, 327–362. https://doi.org/10.1146/annurev.ecolsys.30.1.327
   Google Scholar
• Yonezawa, T., Segawa, T., Mori, H., Campos, P. F., Hongoh, Y., Endo, H., Akiyoshi, A., Kohno, N., Nishida, S., Wu, J., Jin, H., Adachi, J., Kishino, H., Kurokawa, K., Nogi, Y., Tanabe, H., Mukoyama, H., Yoshida, K., Rasoamiaramanana, A., Yamagishi, S., Hayashi, Y., Yoshida, A., Koike, H., Akishinonomiya, F., Willerslev, E., & Hasegawa, M. (2017). Phylogenomics and morphology of extinct paleognaths reveal the origin and evolution of the ratites. Current Biology, 27(1), 68–77. doi:10.1016/j.cub.2016.10.029
   PubMed Web of Science ®Google Scholar
• Zacarías, G. G., de la Fuente, M. S, Fernández, M. S., & Zurita, A. E. (2013). 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(3), 298–318. https://doi.org/10.5710/AMGH.05.03.2013.549
   Web of Science ®Google Scholar