Molecular systematics and biogeography of the Hemigalinae civets (Mammalia, Carnivora)

  • Géraldine Veron Institut de Systématique, Evolution, Biodiversité, UMR 7205 ISYEB, CNRS MNHN UPMC EPHE, Muséum national d’Histoire naturelle, Sorbonne Universités, CP 51, 57 rue Cuvier, 75231 Paris Cedex 05
  • Céline Bonillo Service de Systématique moléculaire, UMS CNRS 2700, Muséum national d’Histoire naturelle, CP 26, 57 rue Cuvier, 75231 Paris Cedex 05
  • Alexandre Hassanin Institut de Systématique, Evolution, Biodiversité, UMR 7205 ISYEB, CNRS MNHN UPMC EPHE, Muséum national d’Histoire naturelle, Sorbonne Universités, CP 51, 57 rue Cuvier, 75231 Paris Cedex 05
  • Andrew P. Jennings SMALL CARNIVORES – Research and Conservation, 83 St. Lawrence Street, Portland, 04101 Maine
Keywords: Southeast Asia, phylogeography, civets, Viverridae, molecular systematics


Due to the difficulty in obtaining samples, the systematics of the Hemigalinae civets has not been fully resolved. The aim of this study was to clarify the relationships of the species and the intraspecific diversity within this subfamily, and to explore the environmental factors that might have affected its evolution. Using two mitochondrial and two nuclear markers, we confirmed that the Hemigalinae comprises Owston’s civet, the otter civet, Hose’s civet and the banded civet, but also the Sulawesi palm civet (formerly included in the Paradoxurinae). Our study showed that the banded and Owston’s civets are sister species, and suggested that Hose’s civet is sister to these two. Within the banded civet, we observed a high divergence between individuals from the Mentawai Islands and those from Sumatra and Borneo (while the latter two were not strongly divergent), likely due to the deep sea channel between the Mentawai Islands and Sumatra. Unexpectedly, the Sumatran and Peninsular Malaysian individuals were not closely related, despite the fact that these two regions have repeatedly been connected during the last glaciations. No high polymorphism was found within Owston’s civet, although three groups were obtained: southern China, northern Vietnam and central Vietnam, which might be related to Pleistocene climatic fluctuations.


Agnarsson I., Kuntner M. & May-Collado L.J. 2010. Dogs, cats, and kin: A molecular species-level phylogeny of Carnivora. Molecular Phylogenetics and Evolution 54: 726–745.

Alfaro M.E., Zoller S. & Lutzoni F. 2003. Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution 20: 255–266.

Bandelt H.J, Forster P. & Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

Bird M.I., Taylor D. & Hunt C. 2005. Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Science Reviews 24: 2228–2242.

Cannon C.H., Morley R.J. & Bush A.B.G. 2009. The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proceedings of the National Academy 106: 11188–11193.

Corbet G. & Hill J. 1992. The Mammals of the Indomalayan Region. Oxford University Press, Oxford.

Corlett R.T. 2009. The Ecology of Tropical East Asia. Oxford University Press, Oxford.

Coudrat C.N.Z., Nanthavong C., Sayavong S., Johnson A., Johnston J.B. & Robichaud W.G. 2014. Conservation importance of Nakai-Nam Theun National Protected Area, Laos, for small carnivores based on camera trap data. Raffles Bulletin of Zoology 62: 31–49.

Cracraft J., Feinstein J., Vaughn J. & Helm-Bychowski K. 1998. Sorting out tigers (Panthera tigris): mitochondrial sequences, nuclear inserts, systematics, and conservation genetics. Animal Conservation 1: 63–74.

Darriba D., Taboada G.L., Doallo R., Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.

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. Systematic Biology 63: 879–901.

Esselstyn J.A., Oliveros C.H., Moyle R.G., Peterson A.T., McGuire J.A. & Brown R.M. 2010. Integrating phylogenetic and taxonomic evidence illuminates complex biogeographic patterns along Huxley’s modification of Wallace’s Line. Journal of Biogeography 37: 2054–2066.

Felsenstein J. 1978. Cases in which parsimony or compatibility methods can be positively misleading. Systematic Zoology 27: 401–410.

Gaubert P. & Cordeiro-Estrela P. 2006. Phylogenetic systematics and tempo of evolution of the Viverrinae (Mammalia, Carnivora, Viverridae) within feliformians: Implications for faunal exchanges between Asia and Africa. Molecular Phylogenetics and Evolution 41: 266–278.

Gaubert P., Fernandes C.A., Bruford M.W. & Veron G. 2004a. Genets (Carnivora, Viverridae) in Africa: an evolutionary synthesis based on cytochrome b sequences and morphological characters. Biological Journal of the Linnean Society 81: 589–610.

Gaubert P., Tranier M., Delmas A.S., Colyn M. & Veron G. 2004b. First molecular evidence for reassessing phylogenetic affinities between genets (Genetta) and the enigmatic genet-like taxa Osbornictis, Poiana and Prionodon (Carnivora, Viverridae). Zoologica Scripta 33: 117–129.

Gaubert P., Wozencraft W.C., Cordeiro-Estrela P. & Veron G. 2005. Mosaic of convergences, noise and misleading morphological phylogenies: what’s in a viverrid-like carnivoran? Systematic Biology 54: 865–894.

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. Proceedings of the American Philosophical Society 81: 309–392.

Haig S.M. 1998. Molecular contributions to conservation. Ecology 79: 413–425.

Hall R. 2001. Cenozoic reconstructions of SE Asia and the SW Pacific: changing patterns of land and sea. In: Metcalfe I., Smith J.M.B., Morwood M. & Davidson I.D. (eds) Faunal and Floral Migrations and Evolution in SE Asia–Australasia: 35–56. Swets & Zeitlinger Publishers, Lisse, the Netherlands.

Hall T.E. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.

Isaac N.J.B., Turvey S.T., Collen B., Waterman C. & Baillie J.E.M. 2007. Mammals on the EDGE: Conservation priorities based on threat and phylogeny. PLoS ONE 2: e296.

IUCN 2015. The IUCN Red List of Threatened Species 2015. Available from [accessed 04 January 2016].

Jennings A.P. & Veron G. 2009. Family Viverridae. In: Wilson D. & Mittermeier R.A. (eds) Handbook of the Mammals of the World, Volume 1, Carnivores: 174–223. Lynx Edicions, Barcelona.

Jennings A.P., Mathai J., Brodie J., Giordano A.J. & Veron G. 2013. Predicted distributions and conservation status of two threatened Southeast Asian small carnivores: the banded civet and Hose’s civet. Mammalia 77: 261–671.

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

Masuda R., Kaneko Y., Siriaroonrat B., Subramaniam V. & Hamachi M. 2008. Genetic variations of the masked palm civet Paguma larvata, inferred from mitochondrial cytochrome b sequences. Mammal Study 33: 19–24.[19:GVOTMP]2.0.CO;2

Meijaard E. 2003. Mammals of south-east Asian islands and their Late Pleistocene environments. Journal of Biogeography 30: 1245–1257.

Meijaard E. 2009. Solving mammalian riddles along the Indochinese–Sundaic zoogeographic transition: new insights from mammalian biogeography. Journal of Biogeography 36: 801–802.

Meijaard E. & Sheil D. 2008. The persistence and conservation of Borneo’s mammals in lowland rain forests managed for timber: observations, overviews and opportunities. Ecological Research 23: 21–34.

Moritz C. 1994. Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology 3: 401–411.

Patou M.L., Debruyne R., Jennings A.P., Zubaid A., Rovie-Ryan J.J. & Veron G. 2008. Phylogenetic relationships of the Asian palm civets (Hemigalinae & Paradoxurinae, Viverridae, Carnivora). Molecular Phylogenetics and Evolution 47: 883–892.

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). Journal of Zoology 278: 218–230.

Patou M.L., Wilting A., Gaubert P., Esselstyn J.A., Cruaud C., Jennings A.P., Fickel J. & Veron G. 2010. Evolutionary history of the Paradoxurus palm civets – a new model for Asian biogeography. Journal of Biogeography 37: 2077–2097.

Pocock R.I. 1933. The rarer genera of oriental Viverridae. Proceedings of the Zoological Society of London 1933: 969–1035.

Rambaut A. 2012. Figtree Version 1.4.0. Available from [accessed 30 Sep. 2013].

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. Systematic Biology 61: 539–542.

Ryder O.A. 1986. Species conservation and systematics: the dilemma of subspecies. Trends in Ecology and Evolution 1: 9–10.

Sargis E.J., Woodman N., Morningstar N.C., Reese A.T. & Olson L.E. 2014. Island history affects faunal composition: the treeshrews (Mammalia: Scandentia: Tupaiidae) from the Mentawai and Batu Islands, Indonesia. Biological Journal of the Linnean Society 111: 290–304.

Sathiamurthy E. & Voris H.K. 2006. Maps of Holocene sea level transgression and submerged lakes on the Sunda Shelf. The Natural History Journal of Chulalongkorn University Suppl. 2: 1–43.

Sato J., Hosoda T., Wolsan M., Tsuchiya K., Yamamoto M. & Suzuki H. 2003. Phylogenetic relationships and divergence times among mustelids (Mammalia: Carnivora) based on nucleotide sequences on the nuclear interphotoreceptor retinoid binding protein and mitochondrial cytochrome b genes. Zoological Science 20: 243–264.

Schreiber A., Wirth R., Riffel M. & Van Rompaey H. 1989. Weasels, Civets and Mongooses, and their Relatives. An Action Plan for the Conservation of Mustelids and Viverrids. IUCN/SSC Mustelid and Viverrid Specialist Group, Gland.

Shekelle M., Meier R., Wahyu I., Wirdateti & Ting N. 2010. Molecular phylogenetics and chronometrics of Tarsiidae based on 12S mtDNA haplotypes: Evidence for Miocene origins of crown tarsiers and numerous species within the Sulawesian clade. International Journal of Primatology 31: 1083–1106.

Simmons M.P. 2012. Radical instability and spurious branch support by likelihood when applied to matrices with non-random distributions of missing data. Molecular Phylogenetics and Evolution 62: 472–484.

Stelbrink B., Albrecht C., Hall R. & Von Rintelen T. 2012. The biogeography of Sulawesi revisited: Is there evidence for a vicariant origin of taxa on Wallace’s “anomalous island”? Evolution 66: 2252–2271.

Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

Tu V.T., Csorba G., Ruedi M., Furey N.M., Son N.T., Thong V.D., Bonillo C. & Hassanin A. 2017. Comparative phylogeography of bamboo bats of the genus Tylonycteris (Chiroptera, Vespertilionidae) in Southeast Asia. European Journal of Taxonomy 274: 1–38.

Veron G. 1994. Méthodes de Recherche en Biotaxonomie des Mammifères Carnivores. Confrontation des Méthodes de Phylogénie Traditionnelle et Moléculaire dans la Recherche de la Position Systématique de Cryptoprocta ferox (Aeluroidea). PhD Dissertation, Muséum national d’Histoire naturelle, France.

Veron G. 1995. La position systématique de Cryptoprocta ferox (Carnivora). Analyse cladistique des caractères morphologiques de carnivores Aeluroidea actuels et fossiles. Mammalia 59: 551–582.

Veron G. 2001. The palm civets of Sulawesi. Small Carnivore Conservation 24: 13–14.

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: 64–91. Cambridge University Press, Cambridge.

Veron G. & Heard S. 2000. Molecular systematics of the Asiatic Viverridae (Carnivora) inferred from mitochondrial cytochrome b sequence analysis. Journal of Zoological Systematics and Evolutionary Research 38: 209–217.

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). Animal Conservation 7: 107–112.

Veron G., Gaubert P., Franklin N., Jennings A.P. & Grassman Jr L.I. 2006. A reassessment of the distribution and taxonomy of the endangered otter civet Cynogale bennettii (Carnivora: Viverridae) of South-east Asia. Oryx 40: 42–49.

Veron G., Patou M.L., Pothet G., Simberloff D. & Jennings A.P.J. 2007. Systematic status and biogeography of the Javan and small Indian mongooses (Herpestidae, Carnivora). Zoologica Scripta 36: 1–10.

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 of the Malay civet Viverra tangalunga (Carnivora: Viverridae) across Southeast Asia: natural or human-mediated dispersal? Zoological Journal of the Linnean Society 170: 917–932.

Veron G., Patou M.L., Debruyne R., Couloux A., Fernandez D.A.P., Wong S.T., Fuchs J. & Jennings A.P. 2015a. Systematics of the Southeast Asian mongooses (Herpestidae, Carnivora): Solving the mystery of the elusive collared mongoose and Palawan mongoose. Zoological Journal of the Linnean Society 173: 236–248.

Veron G., Patou M.L. & Jennings A.P. 2015b. Molecular systematics of the small-toothed palm civet (Arctogalidia trivirgata) reveals a strong divergence of Borneo populations. Mammalian Biology 80: 347–354.

Veron G., Patou M.L., Tóth M., Goonatilake M. & Jennings A.P. 2015c. How many species of Paradoxurus civets are there? New insights from India and Sri Lanka. Journal of Zoological Systematics and Evolutionary Research 53: 161–174.

Voris H.K. 2000. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography 27: 1153–1167.

Willcox D., Do T.H. & Tran Q.P. 2011. Report on the winter–spring survey for small carnivores and pangolins in the Ngoc Son – Ngo Luong Nature Reserve, Hoa Binh Province, Carnivore and Pangolin Conservation Program, Vietnam. Available from[accessed 28 Jan. 2015].

Wilting A. & Fickel J. 2012. Phylogenetic relationship of two threatened endemic viverrids from the Sunda Islands, Hose’s civet and Sulawesi civet. Journal of Zoology 288: 184–190.

Wilting A., Sollmann R., Meijaard E., Helgen K.M. & Fickel J. 2012. Mentawai’s endemic, relictual fauna: is it evidence for Pleistocene extinctions on Sumatra? Journal of Biogeography 39: 1608–1620.

Winnepenninckx B., Backeljau T. & De Wachter R. 1993. Extraction of high molecular weight DNA from molluscs. Trends in Genetics 9: 407.

Woodruff D.S. 2010. Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity. Biodiversity and Conservation 19: 919–941.

Woodruff D.S. & Turner L. 2009. The Indochinese-Sundaic zoogeographic transition: a description and analysis of terrestrial mammal species distributions. Journal of Biogeography 36: 803–821.

Wozencraft C.W. 1989. The phylogeny of the recent Carnivora. In: Gittleman J.L. (ed.) Carnivores: Behavior, Ecology, and Evolution: 495–535. Cornell University Press, Ithaca, New York.

Wozencraft C.W. 2005. Order Carnivora. In: Wilson D.E. & Reeder D.M. (eds) Mammal Species of the World. A Taxonomic and Geographic Reference, 3rd edition: 532–628. The Johns Hopkins University Press, Baltimore.

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.

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. Molecular Phylogenetics and Evolution 35: 483–495.

Yu L., Li Q.W., Ryder O.A. & Zhang Y.P. 2004. Phylogenetic relationships within mammalian order Carnivora indicated by sequences of two nuclear DNA genes. Molecular Phylogenetics and Evolution 33: 694–705.

How to Cite
Veron, G., Bonillo, C., Hassanin, A., & Jennings, A. P. (2017). Molecular systematics and biogeography of the Hemigalinae civets (Mammalia, Carnivora). European Journal of Taxonomy, (285).