Mammalian Biology

, Volume 80, Issue 4, pp 347–354 | Cite as

Molecular systematics of the small-toothed palm civet (Arctogalidia trivirgata) reveals a strong divergence of Bornean populations

  • Géraldine VeronEmail author
  • Marie-Lilith Patou
  • Andrew P. Jennings
Original Investigation


The small-toothed palm civet Arctogalidia trivirgata is a small, arboreal civet belonging to the subfamily Paradoxurinae (Viverridae) that is found in northeast India, southern China, and Southeast Asia. This is an understudied species with a debated taxonomy. Variation in coat colour and pattern has driven authors to describe numerous taxa of this civet species, but no recent taxonomic revision and no intraspecific molecular study have been conducted. We sequenced three mitochondrial and one nuclear markers in order to study the geographical genetic structure of the small-toothed palm civet and to evaluate the genetic divergence between different populations, and we examined various morphological features. Our molecular results showed that the small-toothed palm civet forms two divergent clades: Clade 1: mainland Southeast Asia, Sumatra and nearby small islands, and Java; and Clade 2: Borneo. Further investigations are needed to verify the possible specific status of these two clades. The populations north of the Isthmus of Kra are characterized by a white ear tip and form a separate clade from the populations south of the Isthmus of Kra, but their genetic divergence does not warrant a specific status. The Javan small-toothed palm civet was found to have a low genetic divergence to the nearby populations within Clade 1. Further studies are needed in order to confirm these results and to revise the taxonomy of the small-toothed palm civet.


Asia Biogeography Molecular systematics Palm civets Viverridae 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48.CrossRefGoogle Scholar
  2. Bird, M.I., Taylor, D., Hunt, C, 2005. Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Sci. Rev. 24, 2228–2242.Google Scholar
  3. Brandon-Jones, D., 1996. The Asian Colobinae (Mammalia, Cercopithecidae)as indicators of Quaternary climatic changes. Biol. J. Linn. Soc. 59, 327–350.CrossRefGoogle Scholar
  4. Brandon-Jones, D., 2001. Borneo as a biogeographic barrier to Asian-Australasian migration. In: Metcalfe, I., Smith, J., Morwood, M., Davidson, I. (Eds.), Faunal and Floral Migrations and Evolution in Se Asia-Australasia. A.A. Balkema Publishers, Lisse, pp. 365–372.Google Scholar
  5. Corbet, G.B., Hill, J.E., 1992. The Mammals of the Indomalayan Region: A Systematic Review. Oxford University Press, Oxford.Google Scholar
  6. Cosson, L., Grassman Jr., L.L., Zubaid, A., Vellayan, S., Tillier, A., Veron, G., 2007. Genetic diversity of captive binturongs (Arctictis binturong, Viverridae, Car-nivora): implications for conservation. J. Zool. 271, 386–395.CrossRefGoogle Scholar
  7. de Bruyn, M., Stelbrink, B., Morley, R.J., Hall, R., Carvalho, G.R., Cannon, C.H., van den Bergh, G., Meijaard, E., Metcalfe, I., Boitani, L., Maiorano, L., Shoup, R., von Rintelen, T., 2014. Borneo and Indochina are major evolutionary hotspots for Southeast Asian biodiversity. Syst. Biol. 63, 879–901.CrossRefGoogle Scholar
  8. Eaton, J.A., Wuest, R., Wirth, R., Shepherd, C.R., Semiadi, G., Hall, J., Duckworth, J.W., 2010. Recent records of the Javan small-toothed palm civet Arctogalidia (trivirgata) trilineata. Small Carnivore Conservation 43, 16–22.Google Scholar
  9. Gorog, A.J., Sinaga, M.H., Engstrom, M.D., 2004. Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biol. J. Linn. Soc. 81, 91–109.CrossRefGoogle Scholar
  10. Gregory, W.K., Hellman, H., 1939. On the evolution and major classification of the civets (Viverridae) and allied fossil and recent Carnivora; a phylogenetic study of the skull and dentition. Am. Philos. Soc. 81, 309–392.Google Scholar
  11. Hall, R., 1998. The plate tectonics of Cenozoic SE Asia and the distribution of land and sea. In: Hall, R., Holloway, J.D. (Eds.), Biogeography and Geological Evolution of SE Asia. Backhuys Publishers, Leiden, pp. 99–131.Google Scholar
  12. Hall, R., 2002. Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. J. Asian Earth Sci. 20, 353–431.CrossRefGoogle Scholar
  13. Hall, T.E., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acid. Symp. 41, 95–98.Google Scholar
  14. Heaney, L.R., 1986. Biogeography of mammals in Southeast Asia: estimates of rates of colonization, extinction, and speciation. Biol. J. Linn. Soc. 28, 127–165.CrossRefGoogle Scholar
  15. Jennings, A.P., Veron, G., 2009. Family Viverridae. In: Wilson, D., Mittermeier, R.A. (Eds.), Handbook ofthe Mammals of the World, vol. 1: Carnivores. Lynx edicions, Barcelona, pp. 174–223.Google Scholar
  16. Librado, P., Rosas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle Scholar
  17. Meijaard, E., 2003. Mammals of south-east Asian islands and their Late Pleistocene environments. J. Biogeogr. 30, 1245–1257.CrossRefGoogle Scholar
  18. Meijjard, E., (PhD Thesis) 2004. Solving mammalian riddles. In: A reconstruction of the Tertiary and Quaternary distribution of mammals and their palaeoenviron-ments in island South-East Asia. The Australian National University, Canberra.Google Scholar
  19. Meijaard, E., 2009. Solving mammalian riddles along the Indochinese-Sundaic zoo-geographic transition: new insights from mammalian biogeography. J. Biogeogr. 36, 801–802.CrossRefGoogle Scholar
  20. Patou, M.L., Debruyne, R., Jennings, A.P., Zubaid, A., Rovie-Ryan, J.J., Veron, G., 2008. Phylogenetic relationships ofthe Asian palm civets (Hemigalinae & Paradoxuri-nae, Viverridae, Carnivora). Mol. Phylogenet. Evol. 47, 883–892.CrossRefGoogle Scholar
  21. Patou, M.L., Chen, J., Cosson, L., Andersen, D.H., Cruaud, C, Couloux, A., Randi, E., Zhang, S., Veron, G., 2009. Low genetic diversity in the masked palm civet Paguma larvata (Viverridae). J. Zool. 278, 218–230.CrossRefGoogle Scholar
  22. Patou, M.L., Wilting, A., Gaubert, P., Esselstyn, J.A., Cruaud, C, Jennings, A.P., Fickel, J., Veron, G., 2010. Evolutionary history ofthe Paradoxurus palm civets –a new model for Asian biogeography. J. Biogeogr. 37, 2077–2097.CrossRefGoogle Scholar
  23. Pocock, R.I., 1933. The rarer genera of oriental Viverridae. Proc. Zool. Soc. Lond. 1933, 969–1035.Google Scholar
  24. Pocock, R.I., 1939. The fauna of British India, including Ceylon and Burma. Mammalia, vol. 1. Taylor and Francis, London.Google Scholar
  25. Rambaut, A., 2012. Figtree Version 1.4.0, Available from: (accessed 30.6.14).software/figtree/ (accessed 30.6.14).
  26. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L, Suchard, M.A., Huelsenbeck,J.P., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542.CrossRefGoogle Scholar
  27. Simpson, G.G., 1945. The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85, 1–350.Google Scholar
  28. 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.CrossRefGoogle Scholar
  29. van Bemmel, A.C.V., 1952. Contribution to the knowledge ofthe genera Muntia-cus and Arctogalidia in the Indo-Australian Archipelago (Mammalia, Cervidae & Viverridae). Beaufortia 16, 1–50.Google Scholar
  30. Veron, G., 2010. Phylogeny of the Viverridae and ‘viverrid-like’ feliforms. In: Goswami, A., Friscia, A. (Eds.), Carnivoran Evolution. New Views on Phylogeny, Form and Function. Cambridge University Press, Cambridge, pp. 64–91.CrossRefGoogle Scholar
  31. Veron, G., Heard, S., 2000. Molecular systematics ofthe Asiatic Viverridae (Carnivora) inferred from mitochondrial cytochrome b sequence analysis. J. Zool. Syst. Evol. Res. 38, 209–217.CrossRefGoogle Scholar
  32. Veron, G., Heard Rosenthal, S., Long, B., Roberton, S., 2004. The molecular systematics and conservation of an endangered carnivore, the Owston’s palm civet Chrotogale owstoni (Thomas, 1912) (Carnivora, Viverridae, Hemigalinae). Anim. Conserv. 7, 107–112.CrossRefGoogle Scholar
  33. Veron, G., Patou, M.L., Pothet, G., Simberloff, D., Jennings, A.P., 2007. Systematic status and biogeography of the Javan and small Indian mongooses (Herpestidae, Carnivora). Zool. Scr. 36, 1–10.CrossRefGoogle Scholar
  34. Veron, G., Willsch, M., Dacosta, V., Patou, M.L., Seymour, A., Bonillo, C, Couloux, A., Wong, S.T., Jennings, A.P., Fickel, J., Wilting, A., 2014. The distribution ofthe Malay civet Viverra tangalunga (Carnivora: Viverridae) across Southeast Asia: natural or human-mediated dispersal? Zool. J. Linn. Soc. 170, 917–932.CrossRefGoogle Scholar
  35. Veron, G., Patou, M.L., Debruyne, R., Couloux, A., Fernandez, D.A.P.,Wong, S.T., Fuchs, J., Jennings, A.P., 2015. Systematics ofthe Southeast Asian mongooses (Herpestidae, Carnivora) –solving the mystery ofthe elusive collared mongoose and Palawan mongoose. Zool. J. Linn. Soc. 173, 236–248.CrossRefGoogle Scholar
  36. Veron, G., Patou, M.L., Tóth, M., Goonatilake, M., Jennings, A.P., in press. How many species of Paradoxurus civets are there? New insights from India and Sri Lanka. J. Zool. Syst. Evol. Res.
  37. Voris, H.K., 2000. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J. Biogeogr. 27, 1153–1167.CrossRefGoogle Scholar
  38. Wallace, A.R., 1869. The Malay Archipelago: The Land of the Orang-Utan and the Bird of Paradise. A Narrative of Travel, with Studies of Man and Nature. Macmillan and Co., London.Google Scholar
  39. Wilting, A., Christiansen, P., Kitchener, A.C., Kemp, Y.J.M., Ambu, L., Fickel, J., 2011. Geographical variation in and evolutionary history ofthe Sunda clouded leopard (Neofelis diardi) (Mammalia: Carnivora: Felidae) with the description of a new subspecies from Borneo. Mol. Phylogenet. Evol. 58, 317–328.CrossRefGoogle Scholar
  40. Wilting, A., Fickel, J., 2012. Phylogenetic relationship of two threatened endemic viverrids from the Sunda Islands, Hose’s civet and Sulawesi civet. J. Zool. 288, 184–190.CrossRefGoogle Scholar
  41. Winnepenninckx, B., Backeljau,T., De Wachter, R., 1993. Extraction of high molecular weight DNA from molluscs. Trends Genet. 9, 407.Google Scholar
  42. Woodruff, D.S., Turner, L.M., 2009. The Indochinese-Sundaic zoogeographic transition: a description and analysis of terrestrial mammal species distributions. J. Biogeogr. 36, 802–821.CrossRefGoogle Scholar
  43. Wozencraft, C.W., 2005. Mammal Species ofthe World. ATaxonomic and Geographic Reference, 3rd ed. Smithsonian Institution Press, Washington & London.Google Scholar
  44. Yoder, A.D., Burns, M.M., Zehr, S., Delefosse, T., Veron, G., Goodman, S.M., Flynn, J.J., 2003. Single origin of Malagasy Carnivora from an African ancestor. Nature 421, 734–737.CrossRefGoogle Scholar
  45. Yu, L., Zhang, Y.P., 2005. Phylogenetic studies of pantherine cats (Felidae) based on multiple genes, with novel application of nuclear β-fibrinogen intron 7 to carnivores. Mol. Phylogenet. Evol. 35, 483–495.CrossRefGoogle Scholar
  46. Zachos, F.E., Apollonio, M., Baermann, E.V., Festa-Bianchet, M., Goehlich, U., Habel, J.C., Haring, E., Kruckenhauser, L., Lovari, S., McDevitt, A.D., Pertoldi, C, Roess-ner, G.E., Sanchez-Villagra, M.R., Scandura, M., Suchentrunk, F., 2013. Species inflation and taxonomic artefacts—a critical comment on recent trends in mammalian classification. Mamm. Biol. 78, 1–6.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2015

Authors and Affiliations

  • Géraldine Veron
    • 1
    Email author
  • Marie-Lilith Patou
    • 2
  • Andrew P. Jennings
    • 3
  1. 1.Institut de Systématique, Evolution, Biodiversité, UMR 7205 ISYEB, CNRS MNHN UPMC EPHE, Muséum National d’Histoire NaturelleSorbonne Universités, CP 51Paris Cedex 05France
  2. 2.Biotope, Recherche & DéveloppementMèzeFrance
  3. 3.SMALL CARNIVORESResearch and ConservationPortlandUSA

Personalised recommendations