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Mammalian Biology

, Volume 81, Issue 2, pp 163–175 | Cite as

Mitogenomics of the mountain tapir (Tapirus pinchaque, Tapiridae, Perissodactyla, Mammalia) in Colombia and Ecuador: Phylogeography and insights into the origin and systematics of the South American tapirs

  • Manuel Ruiz-GarcíaEmail author
  • Armando Castellanos
  • Luz Agueda Bernal
  • Myreya Pinedo-Castro
  • Franz Kaston
  • Joseph M. Shostell
Original Investigation

Abstract

We sampled 45 Andean mountain tapirs (Tapirus pinchaque) from Colombia and Ecuador and sequenced 15 mitochondrial genes (two rRNAand 13 protein codifying genes)-making up 13,939 base pairs, approximately 83.1% of the total mitochondrial DNA’s length. The overall sample had low to medium levels of nucleotide diversity with diversity slightly higher for the Colombian population. Both populations experienced high historical gene flow and our genetic heterogeneity analyses revealed a low genetic differentiation between them. Therefore, we did not detect any molecular subspecies, or significantly different evolutionary units for T. pinchaque. This species experienced a population expansion in the last 100,000 years but this expansion was more pronounced in the Ecuadorian population especially in the last 10,000 years, whereas the Colombian population underwent a strong bottleneck in the last 5,000 years. There was no significant spatial trend in genetic structure for the mountain tapir in Colombia and Ecuador. Phylogenetic analyses did not detect any important geographic clade within this species. Temporal split between T. pinchaque and T. terrestris might have occurred around 7-1.5 million years ago (MYA). T. pinchaque and T. terrestris+ T. kabomani are two monophyletic clades, suggesting that T. kabomani is not a full species.

Keywords

Tapirus pinchaque Mitochondrial DNA Genetic diversity Spatial genetic structure Phylogenetic analyses 

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References

  1. Akaike, H., 1974. A new look at the statistical model identification. IEEE Trans. Autom. Control AC-19, 716–723.Google Scholar
  2. Ashley, M.V., Norman, J.E., Stross, L, 1996. Phylogenetic analysis of the perios-sodactylan family Tapiridae using mitochondrial cytochrome c oxidase (COII) sequences, J. Mammal. Evol. 3, 315–326.CrossRefGoogle Scholar
  3. Barongi, R.A., 1993. Husbandry and conservation of tapirs Tapirus spp, Int. Zoo Yb. 32, 7–15.CrossRefGoogle Scholar
  4. Bensasson, D., Zhang, D.X., Hartl, D.L., Hewitt, G.M., 2001. Mitochondrial pseudo-genes: evolution’s misplaced witnesses, Trends Ecol. Evol. 16, 314–321.PubMedCrossRefGoogle Scholar
  5. Benton, M., 1991. The Rise of Mammals. Crescent Books, New York.Google Scholar
  6. Bohonak, A.J., 2002. IBD (Isolation by Distance): a program for analyses of isolation by distance, J. Hered. 93, 153–154.CrossRefGoogle Scholar
  7. Brooks, D.M., Bodmer, R.E., Matola, S., 1997. Tapir-Status Survey and Conservation Action Plan. IUCN/SSC Tapir Specialist Group, IUCN Gland & Cambridge.Google Scholar
  8. Bush, G.L., 1981. Stasipatric speciation and rapid evolution in animals. In: Atchley, W.R., Woodruff, D.S. (Eds.), Evolution and Speciation. Essays in Honor of M.J. D. White. Cambridge University Press, Cambridge, USA, pp. 201–218.Google Scholar
  9. Cavelier,J., Lizcano, D., Yerena, E., Downer, C, 2010. The mountain tapir (Tapirus pin-chaque) and Andean bear (Tremarctos ornatus): two charismatic, large mammals in South American tropical montane cloud forests. In: Bouijnacel, LA, Scabena, F.N., Hamilton, L.S. (Eds.), Tropical Montane Cloud Forests: Science for Conservation and Management. Cambridge University Press, Cambridge, USA, pp. 172–181.Google Scholar
  10. Cozzuol, M.A., Clozato, C.L., Holanda, E.C., Rodrigues, F.H.G., Nienow, S., Thoisy, B., Redondo, R.A.F., Santos, F.R., 2013. A new species of tapir from the Amazon, J. Mammal. 94, 1331–1345.CrossRefGoogle Scholar
  11. Downer, C.C., 2001. Observations on the diet and habitat of the mountain tapir (Tapirus pinchaque), J. Zool. 254, 279–291.CrossRefGoogle Scholar
  12. Drummond, A.J., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.Google Scholar
  13. Drummond, A.J., Ho, S.Y.W., Phillips, M.J., Rambaut, A., 2006. Relaxed phylogenetics and dating with confidence. PLOS Biol. 4, e88.CrossRefGoogle Scholar
  14. Excoffier, L, Smouse, P.E., Quattro, J.M., 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data, Genetics 131, 479–491.PubMedPubMedCentralGoogle Scholar
  15. Excoffier, L, Lischer, H.E.L., 2010. Arlequin suite ver3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour. 10, 564–567.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Felsenstein,J., 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach, J. Mol. Evol. 17, 368–376.PubMedCrossRefGoogle Scholar
  17. Ferrero, B.S., Noriega, J.I., 2007. A new upper Pleistocene tapir from Argentina: remarks on the phylogenetics and diversification of Neotropical Tapiridae, J. Vert. Paleontol. 27, 504–511.CrossRefGoogle Scholar
  18. Frisson, G.C., 1998. Paleoindian large mammal hunters on the plains of North America, Proc. Natl. Acad. Sci. U.S.A. 95, 14,576–14,583.CrossRefGoogle Scholar
  19. Haffer, J., 1970. Geologic-climatic history and zoogeographic significance of the Uraba region in northwestern Colombia, Caldasia 10, 603–636.Google Scholar
  20. Hershkovitz, P., 1954. Mammals of Northern Colombi, Preliminary Report no. 7. Tapirs (genus Tapirus), with a systematic review of American species. Proc. U.S. Nat. Mus. 103, 465–496.Google Scholar
  21. Hershkovitz, P., 1966. Mice, land bridges and Latin American faunal interchange. In: Wenzel, R.L., Tipton, V.J. (Eds.), Ectoparasites of Panama. Field Museum of Natural History, Chicago, pp. 725–751.Google Scholar
  22. Holanda, E.C., Ferigolo, J., Ribeiro, A.M., 2011. New Tapirus species (Mammalia: Peris-sodactyla: Tapiridae) from the upper Pleistocene of Amazonia, Brazil, J. Mammal. 92, 111–120.CrossRefGoogle Scholar
  23. Holanda, E.C., Ferrero, B.C., 2013. Reappraisal of the genus Tapirus (Perissodactyla, Tapiridae): systematics and phylogenetic affinities of the South Americantapirs, J. Mammal. Evol. 20, 33–44.CrossRefGoogle Scholar
  24. Houck, M.L., Kingswood, S.C., Kumamoto, A.T., 2000. Comparative cytogenetics of tapirs, genus Tapirus (Perissodactyla, Tapiridae), Cytogenet. Cell Genet. 89, 110–115.PubMedCrossRefPubMedCentralGoogle Scholar
  25. Hudson, R.R., Boss, D.D., Kaplan, N.L., 1992. A statistical test for detecting population subdivision, Mol. Biol. Evol. 9, 138–151.PubMedGoogle Scholar
  26. Hulbert, R.C., 2010. A new early Pleistocene tapir (Mammalia: Perissodactyla) from Florida, with a review of Blancan tapirs from the state, Bull. Florida Museum Nat. Hist. 49, 67–126.Google Scholar
  27. Hulbert, R.C., Wallace, S.C., 2005. Phylogenetic analysis of late Cenozoic Tapirus (Mammalia, Perissodactyla). J. Vert. Paleontol. 25 (Suppl. 3), 72A.Google Scholar
  28. Kartavtsev, Y., 2011. Divergence at Cyt-b and Co-1 mtDNA genes on different tax-onomic levels and genetics of speciation in animals, Mitochondrial DNA 22, 55–65.PubMedCrossRefGoogle Scholar
  29. Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol. 16, 111–120.PubMedPubMedCentralCrossRefGoogle Scholar
  30. King, M., 1993. Species Evolution. Cambridge University Press, Cambridge.Google Scholar
  31. Lewis, H., 1966. Speciation in flowering plants, Science 152, 167–172.PubMedCrossRefGoogle Scholar
  32. Librado, P., Rozas,J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics 25, 1451–1452, http://dx.doi.org/10.1093/ bioinformatics/btp187.CrossRefGoogle Scholar
  33. Lizcano, D.J.V., Pizarro, J., Cavelier, J., Carmona, J., 2002. Geographic distribution and population size of the mountain tapir (Tapirus pinchaque) in Colombia, J. Biogeogr. 28, 1–9.Google Scholar
  34. Lizcano, D.J., Guarnizo, A., Suárez, J., Flores, F.K., Montenegro, O., 2006. Danta de páramo Tapirus pinchaque. In: Rodríguez-M, J.V., Alberico, M., Trujillo, F., for- genson, J. (Eds.), Libro rojo de los mamíferos de Colombia. Serie libros rojos de especies amenazadas de Colombia. Conservación Internacional Colombia, Ministerio de Ambiente, Vivienda y Desarrollo Territorial, Bogotá, Colombia, 173 pp.Google Scholar
  35. Mantel, N.A., 1967. The detection of disease clustering and a generalized regression approach, Cancer Res. 27, 209–220.PubMedGoogle Scholar
  36. Mau, B., 1996. Bayesian Phylogenetic Inference via Markov Chain Monte Carlo Methods. University of Wisconsin, Madison.Google Scholar
  37. Mau, B., Newton, M., Larget, B., 1999. Bayesian phylogenetic inference via Markov chain Monte Carlo methods, Biometrics 55, 1–12.PubMedCrossRefGoogle Scholar
  38. Norman, J., Ashley, M., 2000. Phylogenetics of Peryssodactyla and tests of the molecular clock, J. Mol. Evol. 50, 11–21.PubMedCrossRefGoogle Scholar
  39. Pinho, G.M., Goncalves da Silva, A., Hrbeck, T., Farias, I.P., 2013. Comportamento Social de antas (Tapirus terrestris): Relacoes de parentesco em uma paisagem fragmentada, Amazonia Central, Brasil. In: I Congreso Latinoamericano de tapires, 8–11 May 2013, Puyo-Pastaza, Ecuador.Google Scholar
  40. Posada, D., Crandall, K.A., 1998. MODELTEST: testing the model of DNA substitution, Bioinformatics 14, 817–818.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Rannala, B., Yang, Z., 1996. Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference, J. Mol. Evol. 43, 304–311.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Rothlisberger, F., 1987. 10,000 jahregletschergeschichte dererde. Verlag Sauerlan-der, Aarau, Switzerland, pp. 1–225.Google Scholar
  43. Ruiz-García, M., Vásquez, C, Pinedo-Castro, M., Sandoval, S., Kaston, F., Thoisy, B., Shostell, J.M., 2012. Phylogeography of the mountain tapir (Tapirus pinchaque) and the Central American tapir (Tapirus bairdii) and the molecular origins of the three South-American tapirs. In: Anamthawat-Jónsson, K. (Ed.), Current Topics in Phylogenetics and Phylogeography of Terrestrial and Aquatic Systems. InTech, Rijeka, Croatia, pp. 83–116.Google Scholar
  44. Ruiz-García, M., Vásquez, C, Sandoval, S., Kaston, F., Luengas-Villamil, K., Shostell, J.M., 2015. Phylogeography and spatial structure of the lowland tapir (Tapirus terrestris, Perissodactyla: Tapiridae) in South America. Mitochondrial DNA 26, 1–9, http://dx.doi.org/10.3109/19401736.2015.1022766 (online).Google Scholar
  45. Schauenberg, P., 1969. Contribution a letude du Tapir pinchaque, Tapirus pinchaque Roulin 1829, Rev. Suisse Zool. 76, 211–256.CrossRefGoogle Scholar
  46. Simpson, B.B., 1979. Quaternary biogeography of the high montane regions of South America. In: Duellman, W.E. (Ed.), The South American Herpetofauna: Its Origin, Evolution and Dispersal. Monograph of the Museum of Natural History No. 7. University of Kansas, Lawrence, pp. 157–188.Google Scholar
  47. Sokal, R.R., Rohlf, F.J., 1981. Biometry: The Principles and Practice of Statistics in Biological Research, 2nd ed. Freeman, San Francisco.Google Scholar
  48. Swofford, D.L, 2002. PAUP*. Phylogenetic analysis using parsimony and other methods., pp. 1–142 https://doi.org/paup.csit.fsu.edu
  49. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol. 28, 2731–2739.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Thalmann, O., Hebler, J., Poinar, H.N., Paabo, S., Vigilant, L, 2004. Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other apes, Mol. Ecol. 13, 321–335.PubMedCrossRefGoogle Scholar
  51. Thoisy, B., Goncalves da Silva, A., Ruiz-García, M., Tapia, A., Ramirez, O., Arana, M., Quse, V., Paz-y-Mino, C, Tobler, M., Pedraza, C, Lavergne, A., 2010. Population history, phylogeography, and conservation genetics of the last Neotropical mega-herbivore, the Lowland tapir (Tapirus terrestris), BMC Evol. Biol. 10, 278–295.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Thompson, L.G., Mosley, E., Davies, M.E., Lin, P.N., Henderson, K.A., Coledal, J., Bolzan, J.F., Liu, K.B., 1995. Huascarán, Perú, Science 269, 46–50.PubMedCrossRefGoogle Scholar
  53. Tirira, D., 2011. Libro Rojo de los Mamíferos del Ecuador. Publicación especial de los Mamíferos del Ecuador No. 8. Pontificia Universi-dad Católica del Ecuador and Ministerio de Medio Ambiente, Quito, Ecuador.Google Scholar
  54. Vaidya, G., Lohman, D.J., Meier, R., 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information, Cladistics 27, 171–180.CrossRefGoogle Scholar
  55. Van der Hammen, T., 2001. Paleoecology of Amazonia. In: Guimaraes Vieira, I.C., Silva, J.M.C., Oren, D.C., D’Incao, M.A.D. (Eds.), Diversidade biológica e cultural da Amazonia. Museu Paraense Emilio Goeldi, Belem, Brazil, pp. 19–44.Google Scholar
  56. Van der Hammen, T., Cleff, A.M., 1992. Holocene changes of rainfall and river discharge in northern South America and the El Nino phenomenon, Erdkunde 46, 252–256.Google Scholar
  57. Van Geel, B., van der Hammen, T., 1973. Upper Quaternary vegetational and climatic sequence of the Fúquene area (Eastern Cordillera, Colombia), Palaeogeogr. Palaeoclimatol. Palaeoecol. 14, 9–92.CrossRefGoogle Scholar
  58. Voss, R.S., Helgen, K.M., Jansa, S.A., 2014. Extraordinary claims require extraordinary evidence: a comment on Cozzuol et al, (2013). J. Mammal. 95, 893–898.CrossRefGoogle Scholar
  59. White, M.J.D., 1968. Models of speciation, New concepts suggest that the classical sympatric and allopatric models are not the only alternatives. Science 159, 1065–1070.Google Scholar
  60. White, M.J.D., 1978. Modes of Speciation. W.H. Freeman, San Francisco.Google Scholar
  61. Wright, S., 1951. The genetical structure of populations, Ann. Eugen. 15, 323–354.PubMedCrossRefPubMedCentralGoogle Scholar
  62. Zachos, F.E., 2015. Tree thinking and species delimitation: guidelines for taxonomy and phylogenetic terminology. Mammal. Biol., http://dx.doi.org/10.1016/j. mambio.2015.10.002 (in press; available online 22 October 2015).Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2015

Authors and Affiliations

  • Manuel Ruiz-García
    • 1
    Email author
  • Armando Castellanos
    • 2
  • Luz Agueda Bernal
    • 1
  • Myreya Pinedo-Castro
    • 1
  • Franz Kaston
    • 3
  • Joseph M. Shostell
    • 4
  1. 1.Laboratorio de Genética de Poblaciones-Biología Evolutiva, Unidad de GenéticaDepartamento de Biología, Facultad de Ciencias, Pontificia Universidad JaverianaBogotáColombia
  2. 2.Andean Bear FundationQuitoEcuador
  3. 3.Fundación NativaBogotáColombia
  4. 4.Department of Math Science and TechnologyUniversity of Minnesota CrookstonCrookstonUSA

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