Skip to main content Skip to main navigation menu Skip to site footer
Type: Articles
Published: 2012-04-26
Page range: 56–66
Abstract views: 180
PDF downloaded: 2

Genetic and shell-shape analyses of Orlitia borneensis (Testudines: Geoemydidae) reveal limited divergence among founders of the European zoo population

Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-12844, Prague 2, Czech Republic
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-12844, Prague 2, Czech Republic
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-12844, Prague 2, Czech Republic
Prague ZOO, U Trojského Zámku 3, CZ-171 00 Prague 7, Czech Republi
Prague ZOO, U Trojského Zámku 3, CZ-171 00 Prague 7, Czech Republi
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-12844, Prague 2, Czech Republic
Ex-situ Captive Breeding Centre, Jalan Raya Hankam no. 49. Bekasi – Indonesia
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-12844, Prague 2, Czech Republic
Reptilia Ex situ breeding genetic variability cytochrome b nuclear gene R35 phylogeography population expansion

Abstract

The Malaysian Giant Turtle (Orlitia borneensis) is a poorly known turtle with rapidly decreasing numbers in nature in spite of its strong protection on paper. Most individuals of this species kept in European zoos and included in captive breeding programs are confiscates from the illegal trade for food consumption and their geographic provenance is unknown. This study was aimed to assess genetic and phenotypic variation of the founders of this captive population. We sequenced the mitochondrial cytochrome b gene and found 23 haplotypes. We constructed a haplotype network and examined demographic changes by Bayesian skyline plots of the effective population size. The maximum sequence divergence was less than 1.5% and the phylogenetic structure of the haplotypes was supported poorly. A close genetic similarity among sampled turtles was further confirmed by sequencing the nuclear R35 gene, while the geometric morphometrics of the shell-shape were likewise similar. Thus, the examined captive population of O. borneensis may be further treated as a single conservation unit.

References

  1. Auliya, M., Mausfeld, P., Schmitz, A. & Böhme, W. (2002) Review of the reticulated python (Python reticulates Schneider, 1801) with the description of new subspecies from Indonesia. Naturwissenschaften, 89, 201–213.

    Avise, J.C., Bowen, B.W., Lamb, T., Meylan, A.B. & Bermingham, E. (1992) Mitochondrial DNA Evolution at a Turtle’s Pace: Evidence for Low Genetic Variability and Reduced Microevolutionary Rate in the Testudines. Molecular Biology and Evolution, 9, 457–473.

    Bandelt, H.J., Foster, P. & Rohl, A. (1999) Median–joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.

    Bookstein, F.L. (1997) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York, 455 pp.

    Chen, T.-H., Chang, H.-C. & Lue, K.-Y. (2009) Unregulated Trade in Turtle Shells for Chinese Traditional Medicine in East and Southeast Asia: The Case of Taiwan. Chelonian Conservation Biology, 8, 11–18.

    Cheung, S.M. & Dudgeon, D. (2006) Quantifying the Asian turtle crisis: market surveys in southern China, 2000-2003. Aquatic Conservation: Marine and Freshwater Ecosystems, 16, 751–770.

    Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

    Ernst, C.H. & Barbour, R.W. (1989) Turtles of the world. Smithsonian Institution Press, London, 416 pp.

    Felsenstein, J. (1985) Confidence limits on phylogeny: an approach using the bootstrap. Evolution, 39, 783–789.

    Fong, J.J. & Chen, T.H. (2010) DNA evidence for the hybridization of wild turtles in Taiwan: possible genetic pollution from trade animals. Conservation Genetics, 11, 2061–2066.

    Fritz, U., Ayaz, D., Buschbom, J., Kami, H.G., Mazanaeva, L.F., Aloufi, A.A., Auer, M., Rifai, L., Šilić, T. & Hundsdörfer, A.K. (2008b) Go east: phylogeographies discordance of mophology, mitochondrial and nuclear genomic markers and rare hybridization. Journal of Evolutionary Biology, 21, 527–540.

    Fritz, U., Guicking, D., Auer, M., Sommer, R.S., Wink, M. & Hundsdörfer, A.K. (2008a) Diversity of the Southeast Asian leaf turtle genus Cyclemys: how many leaves on its tree of life? Zoologica Scripta, 37, 367–390.

    Fritz, U., Stuckas, H., Vargas-Ramírez, M., Hundsdörfer, A.K., Maran, J. & Päckert, M. (2011) Molecular phylogeny of Central and South American slider turtles: implications for biogeography and systematics (Testudines: Emydidae: Trachemys). Journal of Zoological Systematics and Evolutionary Research, doi 10.1111/j.1439-0469.2011.00647.x

    Fujita, M.K., Engstrom, T.N., Starkey, D.E. & Shaffer, H.B. (2004) Turtle phylogeny: insights from a novel nuclear intron. Molecular Phylogenetics and Evolution, 31, 1031–1040.

    Gong, S., Shi, H., Mo, Y., Auer, M., Vargas-Ramírez, M., Hundsdörfer, A.K. & Fritz, U. (2009) Phylogeography of the endangered black-breasted leaf turtle (Geoemyda spengleri) and conservation implications for other chelonians. Amphibia-Reptilia, 30, 57–62.

    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.

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Iverson, J.B. (1992) A revised checklist with distribution maps of the turtles of the world. Privately printed, Richmond, 363 pp.

    Jiang, Y., Nie, L.W., Huang, W.X., Jing, W.X., Wang, L. Liu & Dai, X.T. (2011) Comparison of complete mitochondrial DNA control regions among five Asian freshwater turtle species and their phylogenetic relationships. Genetics and Molecular Research, 10, 1545–1557.

    Keogh, J.S., Barker, D.G. & Shine, R. (2001) Heavily exploited but poorly known: systematics and biogeography of commercially harvested pythons (Python curtus group) in Southeast Asia. Biological Journal of the Linnean Society, 73, 113–129.

    Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.

    Louys, J. (2007) Limited effect of the Quaternary’s largest super-eruption (Toba) on land mammals from Southeast Asia. Quaternary Science Reviews, 26, 3108–3117.

    Luo, S.-J., Kim, J.-H., Johnson, W.E., van der Walt, J., Martenson, J., Yuhki, N., Miquelle, D.G., Uphyrkina, O., Goodrich, J.M., Quigley, H.B., Tilson, R., Brady, G., Martelli, P., Subramaniam, V., McDougal, C., Hean, S., Huang, S.-Q., Pan, W.S., Karanth, U., Sunquist, M., Smith, J.L.D. & O’Brien, S. (2004) Phylogeography and genetic ancestry of tigers (Panthera tigris). PLoS Biology, 2, 2275–2293.

    Martin, A.P. & Palumbi, S.R. (1993) Body size, metabolic rate, generation time, and the molecular clock. Proceedings of the National Academy of Sciences of the United States of America, 90, 4087–4091.

    Nater, A., Nietlisbach, P., Arora, N., van Schaik, C.P., van Noordwijk, M.A., Willems, E.P., Singleton, I., Wich, S.A., Goossens, B., Warren, K.S., Verschoor, E.J., Perwitasari-Farajallah, D., Pamungkas, J. & Krützen, M. (2011) Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant orangutans (genus: Pongo). Molecular Biology and Evolution, 28, 2275–2288.

    Parham, J.F., Simison, W.B., Kozak, K.H., Feldman, C.R. & Shi, H. (2001) New Chinese turtles: endangered or invalid? A reassessment of two species using mitochondrial DNA, allozyme electrophoresis and known-locality specimens. Animal Conservation, 4, 357–367.

    Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Praschag, P., Holloway, R., Georges, A., Päckert, M., Hundsdörfer, A.K. & Fritz, U. (2009a) A new subspecies of Batagur affinis (Cantor, 1847), one of the world's most critically endangered chelonians (Testudines: Geoemydidae). Zootaxa, 2233, 57–68.

    Praschag, P., Hundsdörfer, A.K. & Fritz, U. (2007) Phylogeny and taxonomy of endangered South and South-east Asian freshwater turtles elucidated by mtDNA sequence variation (Testudines: Geoemydidae: Batagur, Callagur, Hardella, Kachuga, Pangshura). Zoologica Scripta, 36, 429–442.

    Praschag, P., Hundsdörfer, A.K. & Fritz, U. (2009b) Further specimens and phylogenetic position of the recently described leaf turtle species Cyclemys gemeli (Testudines: Geoemydidae). Zootaxa, 2008, 29–37.

    Praschag, P., Sommer, R.S., McCarthy, C., Gemel, R. & Fritz, U. (2008) Naming one of the world's rarest chelonians, the southern Batagur. Zootaxa, 1758, 61–68.

    Praschag, P., Stuckas, H., Päckert, M., Maran, J. & Fritz, U. (2011) Mitochondrial DNA sequences suggest a revised taxonomy of Asian flapshell turtles (Lissemys Smith, 1931) and the validity of previously unrecognized taxa (Testudines: Trionychidae). Vertebrate Zoology, 61, 147–160.

    Rampino, M.R. & Ambrose, S.H. (2000) Volcanic winter in the Garden of Eden: The Toba supereruption and the late Pleistocene human population crash. In: McCoy, F.W. & Heiken, G. (Eds), Volcanic Hazards and Disasters in Human Antiquity. Geological Society of America Special Papers, Boulder, pp 71–82.

    Rehák, I. (2004) Hong Kong turtles, two years after. Gazella, 31, 39–48.

    Rohlf, F.J. (2005) tpsDig, digitize landmarks and outlines, version 2.04, Stony Brook: Department of Ecology and Evolution, State University of New York.

    Russell, A.L., Mendellín, A. & McCracken, F. (2005) Genetic variation and migration in the Mexican free-tailed bat (Tadarida brasiliensis mexicana). Molecular Ecology, 14, 2207–2222.

    Samedi & Iskandar, D.T. (2000) Freshwater turtle and tortoise conservation and utilization in Indonesia. In: van Dijk, P.P., Stuart, B.L., & Rhodin, A.G.J. (Eds), Asian Turtle Trade: proceedings of a workshop on conservation and trade of freshwater turtles and tortoises in Asia. Chelonian Research Monographs 2. Chelonian Research Foundation, Lunenburg, Massachusetts, USA, pp 106–111.

    Sheets, H.D. (2003) IMP, version 6a, Department of Physics, Canisius College, Buffalo, New York.

    Spinks, P.Q., Shaffer, H.B., Iverson, J.B. & McCord, W.P. (2004) Phylogenetic hypotheses for the turtle family Geoemydidae. Molecular Phylogenetics and Evolution, 32, 164–182.

    StatSoft I (2001) STATISTICA (data analysis software system) version 6. Available from www.statsoft.com. (Accessed 24 April 2011).

    Stuart, B.L. & Fritz, U. (2008) Historical DNA from museum type specimens clarifies diversity of Asian leaf turtles (Cyclemys). Biological Journal of the Linnean Society, 94, 131–141.

    Stuart, B.L. & Parham, J.F. (2007) Recent hybrid origin of three rare Chinese turtles. Conservation Genetics, 8, 169–175.

    Stuckas, H. & Fritz, U. (2011) Identity of Pelodiscus sinensis revealed by DNA sequences of an approximately 180-year-old type specimen and a taxonomic reappraisal of Pelodiscus species (Testudines: Trionychidae). Journal of Zoological Systematics and Evolutionary Research, 49, 335–339.

    Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony. Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts.

    Thinh, V.N., Moontrick, A.R., Geissmann, T., Li, M., Ziegler, T., Agil, M., Moisson, P., Nadler, T., Walter, L. & Roos, Ch. (2010) Mitochondrial evidence for multiple radiations in the evolutionary history of small apes. BMC Evolutionary Biology, 10, 74–87.

    Thompson, D.J., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTALX windows interface: flexible strategies for multiple sequence alignments aided by quality analysis tool. Nucleic Acids Research, 24, 4876–4882.

    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.

    Voris, H.K. (2000) Maps of Pleistocene Sea Levels in South East Asia: Shorelines, River Systems, Time Durations. Journal of Biogeography, 27, 1153–1167.

    Wiens, J.J., Kuczynski, C.A. & Stephens, P.R. (2010) Discordant mitochondrial and nuclear gene phylogenies in emydid turtles: implications for speciation and conservation. Biological Journal of the Linnean Society, 99, 445–461.

    Williams, M.A.J., Ambrose, S.H., van der Kaars, S., Ruehlemann, C., Chattopadhyaya, U., Pal, J. & Chauhan, P.R. (2009) Environmental impact of the 73 ka Toba super–eruption in South Asia. Palaeogeography, Palaeoclimatology, Palaeoecology, 284, 295–314.

    Zelditch, M.L., Swiderski, D.L., Sheets, H.D. & Fink W.L. (2004) Geometric morphometrics for biologists: A primer. Elsevier Academic Press, New York and London, 437 pp.

    Zhou, Z.H. & Jiang, Z.G. (2008) Characteristics and risk assessment of international trade in tortoises and freshwater turtles in China. Chelonian Conservation and Biology, 7, 28–36.