Abstract
Using phylogenetic and haplotype network analyses of 2036 bp of mitochondrial DNA, we compare samples of the two hinged terrapin species Pelusios castanoides and P. subniger from continental Africa, Madagascar and the Seychelles to infer their biogeography. Owing to the long independent history of Madagascar and the Seychelles, the populations from those islands should be deeply divergent from their African conspecifics. Seychellois populations of the two species are currently recognized as Critically Endangered endemic subspecies. However, even though we found within P. subniger evidence for a cryptic species from the Democratic Republic of the Congo, all other samples assigned to this species were undifferentiated. This suggests that Malagasy and Seychellois populations of P. subniger were introduced by humans and that the Seychellois subspecies P. s. parietalis is invalid. This has implications for current conservation strategies for the Critically Endangered Seychellois populations and suggests that measures should rather focus on endemic species. The situation of P. castanoides could be different. Samples from Madagascar and the Seychelles are weakly, but consistently, differentiated from continental African samples, and Malagasy and Seychellois samples are reciprocally monophyletic in maximum likelihood analyses. However, due to a lack of samples from central and northern Mozambique and Tanzania, we cannot exclude that identical continental haplotypes exist there.
Similar content being viewed by others
References
Bonnaterre, P. J. (1789). Tableau Encyclopédique et Méthodique des Trois Règnes de la Nature. Erpétologie. Paris: Panckoucke, Hôtel de Thou.
Bour, R. (1978). Les tortues actuelles de Madagascar (République malgache): liste systématique et description de deux sous-espèces nouvelles (Reptilia - Testudines). Bulletin du Société d’Études scientifique de Anjou, Nouvelle Série, 10, 141–154.
Bour, R. (1983). Trois populations endémiques du genre Pelusios (Reptilia, Chelonii, Pelomedusidae) aux îles Seychelles; relations avec les espèces africaines et malgaches. Bulletin du Muséum national d’Histoire naturelle, 4e Série, Section A, 5, 343–382.
Bour, R. (1984). Taxonomy, history and geography of Seychelles land tortoises and fresh-water turtles. In D. R. Stoddart (Ed.), Biogeography and ecology of the Seychelles islands (pp. 281–307). The Hague: Kluwer. Monographiae biologicae, 55.
Bour, R., & Gerlach, J. (2008). Pelusios seychellensis (Siebenrock 1906) – Seychelles mud turtle. In A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, & J. B. Iverson (Eds.), Conservation biology of freshwater turtles and tortoises: A compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group (pp. 018.1–018.3). Lunenburg: Chelonian Research Foundation. Chelonian Research Monographs, 5.
Bringsøe, H., Buskirk, J. R., & Willemsen, R. E. (2001). Testudo marginata Schoepff, 1792 – Breitrandschildkröte. In U. Fritz (Ed.), Handbuch der Reptilien und Amphibien Europas. Band 3/IIIA: Schildkröten I (pp. 291–334). Wiebelsheim: Aula-Verlag.
Caccone, A., Amato, G., Gratry, O. C., Behler, J., & Powell, J. R. (1999). A molecular phylogeny of four endangered Madagascar tortoises based on mtDNA sequences. Molecular Phylogenetics and Evolution, 12, 1–9.
Chambers, P. (2004). A sheltered life: The unexpected history of the giant tortoise. London: John Murray.
Clement, M., Posada, D., & Crandall, K. A. (2000). tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.
Collier, J. S., Sansom, V., Ishizuka, O., Taylor, R. N., Minshull, T. A., & Whitmarsh, R. B. (2008). Age of Seychelles – India break-up. Earth and Planetary Science Letters, 272, 264–277.
Crottini, A., Madsen, O., Poux, C., Strauß, A., Vieites, D. R., & Vences, M. (2012). Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K-T boundary in Madagascar. Proceedings of the National Academy of Sciences of the USA, 109, 5358–5363.
Daniels, S. R. (2011). Reconstructing the colonisation and diversification history of the endemic freshwater crab (Seychellum alluaudi) in the granitic and volcanic Seychelles Archipelago. Molecular Phylogenetics and Evolution, 61, 534–542.
Ernst, C. H., Altenburg, R. G. M., & Barbour, R. W. (2000). Turtles of the world. World biodiversity database, version 1.2. CD-ROM. Amsterdam: Biodiversity Center of ETI.
Fritz, U. (2001). Emys orbicularis (Linnaeus, 1758) – Europäische Sumpfschildkröte. In U. Fritz (Ed.), Handbuch der Reptilien und Amphibien Europas. Band 3/IIIA: Schildkröten I (pp. 343–515). Wiebelsheim: Aula-Verlag.
Fritz, U., & Havaš, P. (2007). Checklist of chelonians of the world. Vertebrate Zoology, 57, 149–368.
Fritz, U., Obst, F.-J., & Günther, R. (1994). Kritischer Typen-Katalog der Schildkrötensammlung (Reptilia: Testudines) des Zoologischen Museums Berlin. Mitteilungen aus dem Zoologischen Museum Berlin, 70, 157–175.
Fritz, U., Auer, M., Bertolero, A., Cheylan, M., Fattizzo, T., Hundsdörfer, A. K., Martín Sampayo, M., Pretus, J. L., Široký, P., & Wink, M. (2006). A rangewide phylogeography of Hermann’s tortoise, Testudo hermanni (Reptilia: Testudines: Testudinidae): implications for taxonomy. Zoologica Scripta, 35, 531–543.
Fritz, U., Harris, D. J., Fahd, S., Rouag, R., Graciá Martínez, E., Giménez Casalduero, A., Široký, P., Kalboussi, M., Jdeidi, T. B., & Hundsdörfer, A. K. (2009). Mitochondrial phylogeography of Testudo graeca in the Western Mediterranean: old complex divergence in North Africa and recent arrival in Europe. Amphibia-Reptilia, 30, 63–80.
Fritz, U., Branch, W. R., Hofmeyr, M. D., Maran, J., Prokop, H., Schleicher, A., Široký, P., Stuckas, H., Vargas-Ramírez, M., Vences, M., & Hundsdörfer, A. K. (2011). Molecular phylogeny of African hinged and helmeted terrapins (Testudines: Pelomedusidae: Pelusios and Pelomedusa). Zoologica Scripta, 40, 115–125.
Fritz, U., Vargas-Ramírez, M., & Široký, P. (2012). Phylogenetic position of Pelusios williamsi and a critique of current GenBank procedures (Reptilia: Testudines: Pelomedusidae). Amphibia-Reptilia, 33, 150–154.
Garrick, R. C., Benavides, E., Russello, M. A., Gibbs, J. P., Poulakakis, N., Dion, K. B., Hyseni, C., Kajdacsi, B., Márquez, L., Bahan, S., Ciofi, C., Tapia, W., & Caccone, A. (2012). Genetic rediscovery of an ‘extinct’ Galápagos giant tortoise species. Current Biology, 22, R10–R11.
Gerlach, J. (2008a). Pelusios castanoides intergularis Bour 1983 – Seychelles yellow-bellied mud turtle, Seychelles chestnut-bellied terrapin. In A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, & J. B. Iverson (Eds.), Conservation biology of freshwater turtles and tortoises: A compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group (pp. 010.1–010.4). Lunenburg: Chelonian Research Foundation. Chelonian Research Monographs, 5.
Gerlach, J. (2008b). Pelusios subniger parietalis Bour 1983 – Seychelles black mud turtle. In A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, & J. B. Iverson (Eds.), Conservation biology of freshwater turtles and tortoises: A compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group (pp. 016.1–016.4). Lunenburg: Chelonian Research Foundation. Chelonian Research Monographs, 5.
Gerlach, J., & Canning, K. L. (2001). Range contractions in the Critically Endangered Seychelles terrapins (Pelusios spp.). Oryx, 35, 313–320.
Giacalone, G., Lo Valvo, M., & Fritz, U. (2009). Phylogeographic link between Sicilian and Corso-Sardinian Testudo h. hermanni confirmed. Acta Herpetologica, 4, 119–123.
Hall, T. A. (1999). bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Harmon, L. J., Melville, J., Larson, A., & Losos, J. B. (2008). The role of geography and ecological opportunity in the diversification of day geckos (Phelsuma). Systematic Biology, 57, 562–573.
Hewitt, J. (1931). Descriptions of some African tortoises. Annals of the Natal Museum, 6, 461–506.
IUCN (2007). IUCN Red List of Threatened Species. Version 2007. http://www.iucnredlist.org. Accessed 31 October 2007.
Iverson, J. B. (1992). A Revised Checklist with Distribution Maps of the Turtles of the World. Richmond: Privately Printed.
Jiang, Z. J., Castoe, T. A., Austin, C. C., Burbrink, F. T., Herron, M. D., McGuire, J. A., Parkinson, C. L., & Pollock, D. D. (2007). Comparative mitochondrial genomics of snakes: extraordinary substitution rate dynamics and functionality of the duplicate control region. BMC Evolutionary Biology, 7, 123.
Kindler, C., Branch, W. R., Hofmeyr, M. D., Maran, J., Široký, P., Vences, M., Harvey, J., Hauswaldt, J. S., Schleicher, A., Stuckas, H., & Fritz, U. (2012). Molecular phylogeny of African hinge-back tortoises (Kinixys): implications for phylogeography and taxonomy (Testudines: Testudinidae). Journal of Zoological Systematics and Evolutionary Research, 50, 192–201.
Klaus, S., Schubart, C. D., Streit, B., & Pfenninger, M. (2010). When Indian crabs were not yet Asian – biogeographic evidence for Eocene proximity of India and Southeast Asia. BMC Evolutionary Biology, 10, 287.
Lescure, J. (1983). Introductions passives et actives de reptiles et d’amphibiens dans les Antilles et les Guyanes. Compté Rendu des Séances de la Société de Biogéographie, 59, 59–70.
MacFarland, C. G., Villa, J., & Toro, B. (1974). The Galápagos giant tortoises (Geochelone elephantopus). I. Status of the surviving populations. Biological Conservation, 6, 118–133.
Measey, G. J., Vences, M., Drewes, R. C., Chiari, Y., Melo, M., & Bourles, B. (2007). Freshwater paths across the ocean: molecular phylogeny of the frog Ptychadena newtoni gives insights into amphibian colonization of oceanic islands. Journal of Biogeography, 34, 7–20.
Nagy, Z. T., Joger, U., Wink, M., Glaw, F., & Vences, M. (2003). Multiple colonization of Madagascar and Socotra by colubrid snakes: evidence from nuclear and mitochondrial gene phylogenies. Proceedings of the Royal Society B, 270, 2613–2621.
Pedall, I., Fritz, U., Stuckas, H., Valdéon, A., & Wink, M. (2011). Gene flow across secondary contact zones of the Emys orbicularis complex in the Western Mediterranean and evidence for extinction and re-introduction of pond turtles on Corsica and Sardinia (Testudines: Emydidae). Journal of Zoological Systematics and Evolutionary Research, 49, 44–57.
Posada, D., & Crandall, K. A. (1998). modeltest: testing the model of DNA substitution. Bioinfomatics, 14, 817–818.
Poulakakis, N., Russello, M., Geist, D., & Caccone, A. (2011). Unravelling the peculiarities of island life: vicariance, dispersal and the diversification of the extinct and extant giant Galápagos tortoises. Molecular Ecology, 21, 160–173.
Ronquist, F., & Huelsenbeck, J. P. (2003). mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
Rowson, B., Tattersfield, P., & Symondson, W. O. C. (2011). Phylogeny and biogeography of tropical carnivorous land-snails (Pulmonata: Streptaxoidea) with particular reference to East Africa and the Indian Ocean. Zoologica Scripta, 40, 85–98.
Samonds, K. A., Godfrey, L. R., Ali, J. R., Goodman, S. M., Vences, M., Sutherland, M. R., Irwin, M. T., & Krause, D. W. (2012). Spatial and temporal arrival patterns of Madagascar’s vertebrate fauna explained by distance, ocean currents, and ancestor type. Proceedings of the National Academy of Sciences of the USA, 109, 5352–5357.
Siebenrock, F. (1906). Schildkröten von Ostafrika und Madagaskar. In A. Voeltzkow (Ed.), Reise in Ostafrika in den Jahren 1903–1905 mit Mitteln der Hermann und Elise geb. Heckmann Wentzel-Stiftung ausgeführt von Professor Dr. Alfred Voeltzkow. Wissenschaftliche Ergebnisse, Band II. Systematische Arbeiten (pp. 1–40 + 5 plates). Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung, Nägele & Dr. Sproesser.
Silva, A., Rocha, S., Gerlach, J., Rocamora, G., Dufrenne, A., & Harris, D. J. (2010). Assessment of mtDNA genetic diversity within the terrapins Pelusios subniger and Pelusios castanoides across the Seychelles islands. Amphibia-Reptilia, 32, 583–588.
Silvestro, D., & Michalak, I. (2011). raxmlgui: a graphical front-end for raxml. Organisms, Diversity and Evolution. doi:10.1007/s13127-011-0056-0.
Stamatakis, A. (2006). raxml-vi-hpc: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
Stoddart, D. R., & Peake, J. F. (1979). Historical records of Indian Ocean giant tortoise populations. Philosophical Transactions of the Royal Society B, 286, 147–161.
Townsend, C. H. (1925). The Galápagos tortoises in their relation to the whaling industry: a study of old logbooks. Zoologica, 4, 55–135.
Townsend, T. M., Tolley, K. A., Glaw, F., Böhme, W., & Vences, M. (2011). Eastward from Africa: paleocurrent-mediated chameleon dispersal to the Seychelles Islands. Biology Letters, 7, 225–228.
Vamberger, M., Corti, C., Stuckas, H., & Fritz, U. (2011). Is the imperilled spur-thighed tortoise (Testudo graeca) native in Sardinia? Implications from population genetics and for conservation. Amphibia-Reptilia, 32, 9–25.
van Dijk, P. P., Iverson, J. B., Shaffer, H. B., Bour, R., & Rhodin, A. G. J. (2011). Turtles of the world, 2011 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status. In A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, & J. B. Iverson (Eds.), Conservation biology of freshwater turtles and tortoises: A compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group (pp. 000.165–000.242). Lunenburg: Chelonian Research Foundation. Chelonian Research Monographs, 5.
Vargas-Ramírez, M., Vences, M., Branch, W. R., Daniels, S. R., Glaw, F., Hofmeyr, M. D., Kuchling, G., Maran, J., Papenfuss, T. J., Široký, P., Vieites, D. R., & Fritz, U. (2010). Deep genealogical lineages in the widely distributed African helmeted terrapin: evidence from mitochondrial and nuclear DNA (Testudines: Pelomedusidae: Pelomedusa subrufa). Molecular Phylogenetics and Evolution, 56, 428–440.
Vences, M., Vieites, D. R., Glaw, F., Brinkmann, H., Kosuch, J., Veith, M., & Meyer, A. (2003). Multiple overseas dispersal in amphibians. Proceedings of the Royal Society B, 270, 2435–2442.
Vences, M., Wanke, S., Vieites, D. R., Branch, W. R., Glaw, F., & Meyer, A. (2004). Natural colonization or introduction? Phylogeographical relationships and morphological differentiation of house geckos (Hemidactylus) from Madagascar. Biological Journal of the Linnean Society, 83, 115–130.
Wagler, J. G. (1830). Natürliches System der Amphibien, mit vorangehender Classification der Säugthiere und Vögel. München: J.G. Cotta’sche Buchhandlung.
Wong, R. A., Fong, J. J., & Papenfuss, T. J. (2010). Phylogeography of the African helmeted terrapin, Pelomedusa subrufa: genetic structure, dispersal, and human introduction. Proceedings of the California Academy of Sciences, 61, 575–585.
Yoder, A. D., & Nowak, M. (2009). Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annual Review of Ecology, Evolution, and Systematics, 37, 405–431.
Zardoya, R., & Meyer, A. (1998a). Complete mitochondrial genome suggests diapsid affinities of turtles. Proceedings of the National Academy of Sciences of the USA, 95, 14226–14231.
Zardoya, R., & Meyer, A. (1998b). Cloning and characterisation of a microsatellite in the mitochondrial control region of the African side-necked turtle, Pelomedusa subrufa. Gene, 215, 149–153.
Acknowledgements
Hynek Prokop allowed sampling of some terrapins in his care. Thanks for samples from the Seychelles go to James Harris and Peter Praschag. Additional samples from Madagascar were supplied by Gerald Kuchling, Jérôme Maran and Emile Rajeriarison. Radim Blažek, Parfait Bora, Jim and Carol Patton, Theo Rajoafiarison, Roger Daniel Randrianiaina, Fanomezana Ratsoavina and Olivier Verneau helped during field work. Anja Rauh processed the samples in the laboratory.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table S1
Samples and outgroups used in the present study. Sample numbers refer to vouchers in the tissue collection of the Museum of Zoology, Senckenberg Dresden, sample codes starting with letters, to the collection of the Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO), Porto (DOC 197 KB)
Rights and permissions
About this article
Cite this article
Fritz, U., Branch, W.R., Gehring, PS. et al. Weak divergence among African, Malagasy and Seychellois hinged terrapins (Pelusios castanoides, P. subniger) and evidence for human-mediated oversea dispersal. Org Divers Evol 13, 215–224 (2013). https://doi.org/10.1007/s13127-012-0113-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-012-0113-3