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Type: Articles
Published: 2011-04-08
Page range: 1–20
Abstract views: 31
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Mitochondrial diversity of the white-toothed shrews (Mammalia, Eulipotyphla, Crocidura) in Vietnam

Lomonosov Moscow State University, Vorobievy Gory, 119992, Russia
Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034, St.Petersburg, Russia Joint Vietnam-Russian Tropical Research and Technological Centre, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi, Vietnam
Canadian Centre of DNA Barcoding, Biodiversity Institute of Ontario, University of Guelph, Сanada
Zoological Museum of Moscow State University, B.Nikitskaya 6, 125009, Russia
Joint Vietnam-Russian Tropical Research and Technological Centre, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi, Vietnam A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr., 33, Moscow 119071, Russia
Mammalia DNA barcodes molecular biodiversity Soricidae Southeast Asia molecular diagnostics cryptic species

Abstract

We explored the patterning of genetic diversity within white-toothed shrews of the genus Crocidura from 14 localities across Vietnam. An analysis of cytochrome oxidase c subunit I (COI) and cytochrome b (cytb) gene fragments from 185 specimens of white-toothed shrews of the genus Crocidura from 14 localities across Vietnam revealed six deeply divergent (p-distance for both COI and cytb >10%) lineages, corresponding to the morphological species C. sokolovi, C. zaitsevi, C. phuquocensis, С . indochinensis, C. tanakae and, C. phanluongi. Crocidura sokolovi was distinct from all other Vietnamese white-toothed shrews (~13% on average for both cytb and COI). In addition to demonstrating the genetic separation of previously described species, substantial cryptic genetic diversity was revealed. Crocidura zaitsevi and C. tanakae each included two subgroups that corresponded to geographically remote localities, while C. indochinensis contained two distinct subgroups that exhibited co-varying patterns of morphological and ecological differentiation, suggesting that the individuals from Sa Pa represent a separate species (provisionally named Crocidura sp. AB1). Mitochondrial data generated for the type specimens of C. phanluongi from Yok Don and Bu Gia Map supported the validity of the species while an additional specimen from Binh Chau, South Vietnam originally referred to C. phanluongi exhibited a deep genetic split (cytb: 8.4%; COI: 8.7%) from a neighbouring population in Yok Don. We propose that the specimen from Binh Chau also represents an undescribed species (provisionally named Crocidura sp. AB2). Our cytb data were then compared to the sequences of 28 species of Crocidura from Southeast Asia available in GenBank, suggesting that three more species occur in northern Vietnam, namely C. wuchihensis, C. attenuata and C. fuliginosa/C. dracula. The discovery of fairly deep genetic divergences among Vietnamese Crocidura illustrates that the understudied and largely undescribed diversity of white-toothed shrews in Southeast Asia requires deeper scrutiny. It also shows the useful insights of mitochondrial markers as to the taxonomic resolution of this enigmatic group of mammals.

References

  1. Abramov, A.V., Jenkins, P.D., Rozhnov, V.V. & Kalinin, A.A. (2008a) Description of a new species of Crocidura (Soricomorpha: Soricidae) from the island of Phu Quoc, Vietnam. Mammalia, 72, 269–272.

    Abramov, A.V., Shchinov, A.V. & Rozhnov, V.V. (2008b) Study of insectivorous mammals in North Vietnam. Contemporary Problems of Ecology, 1, 593–595.

    Abramov, A.V., Kruskop, S.V. & Shchinov, A.V. (2010) Small mammals of the Dalat Plateau, southern Vietnam. Russian Journal of Theriology, 8, 61–73.

    Bannikova, А.A., Lebedev, V.S., Kramerov, D.A. & Zaitsev, M.V. (2006) Phylogeny and systematics of Crocidura suaveolens species group: corroboration and controversy between nuclear and mitochondrial DNA markers. Mammalia, 70, 106–119.

    Bannikova, A.A., Sheftel, B.I., Lebedev, V.S., Aleksandrov, D.Yu. & Muehlenberg, M. (2009) Crocidura shantungensis, a new species for Mongolia and Buryatia. Doklady Biological Sciences, 424, 68–71.

    Borisenko, A.V., Lim, B.K., Ivanova, N.V., Hanner, R.H. & Hebert, P.D.N. (2008) DNA barcoding in surveys of small mammal communities: A field study in Suriname. Molecular Ecology Resources, 8, 471–479.

    Borisenko, A.V., Sones, J.E. & Hebert, P.D.N. (2009) The front-end logistics of DNA barcoding: challenges and prospects. Molecular Ecology Resources, 9, 27–34.

    Can, D.N., Endo, H., Son, N.T., Oshida, T., Canh, L.X., Phuong, D.H., Lunde, D.P., Kawada, S.-I., Hayashida, A. & Sasaki, M. (2008) Checklist of Wild Mammal Species of Vietnam. Institute of Ecology and Biological Resources, Hanoi, 400 pp.

    Carvalho, M.R., Bockmann, F.A., Amorim, D.S., Brand, CRF, Vivo, M., Figueiredo, J.L., Britski, H.A., Pinna, M.C.C., Menezes, N.A., Marques, F.P.L., Papavero, N., Cancello, E.M., Crisci, J.V., McEachran, J.D., Schelly, R.C., Lundberg, J.G., Gill, A.C., Britz, R., Wheeler, Q.D., Stiassny, M.L.J., Parenti, L.R., Page, L.M., Wheeler, W.C., Faivovich, J.,
    Vari, R.P., Grande, L., Humphries, C.J., DeSalle, R., Ebach, M.C. & Nelson, G.J. (2007) Taxonomic Impediment or Impediment to Taxonomy? A Commentary on Systematics and the Cybertaxonomic-Automation Paradigm. Evolutionary Biology, 34, 140–143.

    Clare, E.L., Lim, B.K., Engstrom, M.D., Eger, J.L. & Hebert, P.D.N. (2007) DNA barcoding of Neotropical bats: species identification and discovery within Guyana. Molecular Ecology Notes, 7, 184–190.

    Corbet, G.B. & Hill, J.E. (1992) The Mammals of the Indomalayan Region. Oxford: Oxford University Press.

    deWaard, J.R., Ivanova, N.V., Hajibabaei, M. & Hebert, P.D.N. (2008) Assembling DNA barcodes: analytical protocols. In: Martin, C.C. (Ed.), Environmental Genomics, Methods Molecular Biology, 410, 275–283, Humana Press.

    Dubey, S., Salamin, N., Ohdachi, S.D., Barrière, P. & Vogel, P. (2007) Molecular phylogenetics of Soricidae (Mammalia, Eulipotyphla) reveals timing of transcontinental colonizations. Molecular Phylogenetics and Evolution, 44, 126–137.

    Dubey, S., Salamin, N., Ruedi, M., Barriere, P., Colyn, M. & Vogel, P. (2008) Biogeographic origin and radiation of the Old World crocidurine shrews (Mammalia: Soricidae) inferred from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 48, 953 –963.

    Ellerman J.R. & Morrison-Scott, T.C.S. (1951) Checklist of Palaearctic and Indian Mammals, 1758 to 1946. Trustees of the British Museum (Natural History), London, 810 pp.

    Esselstyn, J.A. & Brown, R.M. (2009) The role of repeated sea-level fluctuations in the generation of shrew (Soricidae: Crocidura) diversity in the Philippine Archipelago Molecular Phylogenetics and Evolution, 53, 171–181.

    Esselstyn, J.A., Timm, R.M. & Brown, R.M. (2009) Do geological or climatic processes drive speciation in dynamic archipelagos? The tempo and mode of diversification in Southeast Asian shrews. Evolution, 63, 2595–2610.

    Francis, CM, Borisenko, AV, Ivanova, NV, Eger, JL, Lim BK, Eger, JL, Lim, BK, Guillén-Serven, A, Kruskop, SV, Mackie, I. & Hebert, P.D.N. (2010) The Role of DNA Barcodes in Understanding and Conservation of Mammal Diversity in Southeast Asia. PLoS ONE, 5(9), e12575.

    Hajibabaei, M., deWaard, J.R., Ivanova, N., Ratnasingham, S., Dooh, R., Kirk, S. & Mackie, P. (2005) Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society of London B Biological Sciences, 360, 1959–1967.

    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.

    Hanner, R (2009) Data Standards for BARCODE Records in INSDC (BRIs). http://www.barcoding.si.edu/PDF/DWG_data_standards-Final.pdf.

    Harris, D.J. (2003) Can you bank on GenBank?. Trends in Ecology & Evolution, 18, 317–319.

    Heaney, L.R. & Timm, R.M. (1983) Systematics and distribution of shrews of the genus Crocidura (Mammalia: Insectivora) in Vietnam. Proceedings of the Biological Society, Washington, 96, 115–120.

    Hebert, P.D.N., Cywinska, A., Ball, S.L. & Waard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, B, 270, 313–321.

    Huynh, D.H., Tien, D.V., Sung, C.V., Anh, P.T. & Khien, H.M. (1994) Checklist of mammals in Vietnam. Publ. House “Science & Technics”, Hanoi, 168 pp.

    Hutterer, R. (2005) Order Soricomorpha. In: Wilson, D.E. & Reeder D.M. (Eds.), Mammals Species of the World. A Taxonomic and Geographic Reference, 3rd ed. The Johns Hopkins University Press, Baltimore, pp. 220–311.

    Ivanova, N.V., deWaard, J.R. & Hebert, P.D.N. (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6, 998–1002.

    Ivanova, N.V. & Grainger, C.M. (2007) CCDB Protocols, Sequencing. Retrieved from http://www.dnabarcoding.ca/CCDB_DOCS/CCDB_Sequencing.pdf on September 24, 2008. vol. 2008. http://www.dnabarcoding.ca/CCDB_DOCS/CCDB_Sequencing.pdf.

    Ivanova, N.V., Zemlak, T.S., Hanner, R.H. & Hebert, P.D.N. (2007) Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes, 7, 44–5548.

    Jenkins, P.D. (1976) Variation in Eurasian shrews of the genus Crocidura (Insectivora: Soricidae). Bulletin of the British Museum (Natural History), Zoology, 30, 271–309.

    Jenkins, P.D., Abramov, A.V., Rozhnov, V.V. & Makarova, O.V. (2007) Description of two new species of white-toothed shrews belonging to the genus Crocidura (Soricomorpha: Soricidae) from the Ngoc Linh Mountain, Vietnam. Zootaxa, 1589, 57–68.

    Jenkins, P.D., Lunde, D.P. & Moncrieff, C.B. (2009) Chapter 10. Descriptions of new species of Crocidura (Soricomorpha: Soricidae) from mainland Southeast Asia, with synopses of previously described species and remarks on biogeography. In: Voss, R.S. & Carleton, M.C. (Eds.), Systematic mammalogy: contributions in honour of Guy G. Musser. Bulletin of the American Museum of Natural History, 331, 356–405.

    Jenkins, P.D., Abramov, A.V., Rozhnov, V.V. & Olsson, A. (2010) A new species of Crocidura (Soricomorpha: Soricidae) from southern Vietnam and north-eastern Cambodia. Zootaxa, 2345, 60–68.

    Jiang, X. & Hoffmann, R.S. (2001) A revision of the white-toothed shrews (Crocidura) of southern China. Journal of Mammalogy, 82, 1059–1079.

    Kuznetsov, G.V. (2006) Mammals of Vietnam. KMK, Moscow, 420 pp.

    Lavrenchenko, L.A., Bannikova, A.A. & Lebedev, V.S. (2009) Shrews (Crocidura spp.) endemic to Ethiopia: recent adaptive radiation of an ancient lineage. Doklady Biological Sciences, 424, 57–60.

    Lunde, D.P., Musser, G.G. & Son, N.T. (2003) A survey of small mammals from Mt Tay Con Linh II, Vietnam, with the description of a new species of Chodsigoa (Insectivora: Soricidae). Mammal Study, 28, 31–46.

    Lunde, D.P., Musser, G.G. & Ziegler, T. (2004) Description of a new species of Crocidura (Soricomorpha: Soricidae, Crocidurinae) from Ke Go Nature Reserve, Vietnam. Mammal Study, 29, 27–36.

    Maddalena, T. (1990) Systematics and biogeography of Afrotropical and Palaearctic shrews of the genus Crocidura (Insectivora: Soricidae):an electrophoretic approach. In: Peters, G. & Hutterer, R. (Eds.), Vertebrates in the Tropics. Museum Alexander Koenig, Bonn, pp. 297–308.

    Maddalena, T. & Ruedi, H. (1994) Chromosomal evolution in the genus Crocidura (Soricidae, Insectivora). In: Merritt, J.F., Kirkland, G.L. & Rose, R.K. (Eds.), Advances in the Biology of Shrews. Special Publication of Carnegie Museum of Natural History, 18, 335–344.

    Meegaskumbura, S., Meegaskumbura, M., Pethiyagoda, R., Manamendra-Arachchi, K. & Schneider, C.J. (2007) Crocidura hikmiya, a new shrew (Mammalia: Soricomorpha: Soricidae) from Sri Lanka. Zootaxa, 1665, 19–30.

    Motokawa, M., Harada, M., Lin, L.K., Koyasu, K. & Hattori, S. (1997) Karyological study of the gray shrew Crocidura attenuata (Mammalia: Insectivora) from Taiwan. Zoological Studies, 36, 70–73.

    Motokawa, M., Yu, H-T. & Harada, M. (2000) Diversification of the white-toothed shrews of the genus Crocidura (Insectivora: Soricidae) in East and Southeast Asia. Mammal Study, 30, 53–64.

    Motokawa, M., Harada, M., Wu, Y., Lin, L.K. & Suzuki, H. (2001) Chromosomal polymorphism in the gray shrew Crocidura attenuata (Mammalia: Insectivora). Zoological Science, 18, 1153–1160.

    Motokawa, M., Suzuki, H. Harada, M., Lin, L.K., Koyasu, K. & Oda, S. (2005) Phylogenetic relationships among East Asian species of Crocidura (Mammalia: Insectivora) inferred from mitochondrial cytochrome b gene sequences. Zoological Science, 17, 497–504.

    Ohdachi, S.D., Iwasa, M.A., Nesterenko, V.A., Abe, H., Masuda, R. & Haberl, W. (2004) Molecular phylogenetics of Crocidura shrews (Insectivora) in East and Central Asia. Journal of Mammalogy, 85, 396–403.

    Ohdachi, S.D., Hasegawa, M., Iwasa, M.A., Vogel, P., Oshida, T., Lin, L.K. & Abe, H. (2006) Molecular phylogenetics of soricid shrews (Mammalia) based on mitochondrial cytochrome b gene sequences: with special reference to the Soricinae. Journal of Zoology, 270, 777–791.

    Pfunder, M., Holzgang, O. & Frey, J.E. (2004) Development of microarray-based diagnostics of voles and shrews for use in biodiversity monitoring studies, and evaluation of mitochondrial cytochrome oxidase I vs. cytochrome b as genetic markers. Molecular Ecology, 13, 1277–1286.

    Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes, 7, 355–364.

    Ruedas, L.A., Salazar-Bravo, J., Dragoo, J.W. & Yates, T.L. (2000) The importance of being earnest: what if anything constitutes a "specimen examined?" Molecular Phylogenetics and Evolution, 17, 129–32.

    Ruedi, M. (1996) Phylogenetic evolution and biogeography of southeast Asian shrews (genus Crocidura: Soricidae). Biological Journal of the Linnean Society, 58, 197–219.

    Ruedi, M. (1998) Protein evolution in shrews. In: Wojcik, M. & Wolsan, M. (Eds), Evolution of shrews. Mammal Research Institute, Polish Academy of Sciences, Bialowieza, 458 pp.

    Ruedi, M., Auberson, M. & Savolainen, V. (1998) Biogeography of Sulawesian shrews: testing for their origin with a parametric bootstrap on molecular data. Molecular Phylogenetics and Evolution, 9, 567–571.

    Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Lab. Press, Cold Spring Harbor, NY, 398 pp.

    Swofford, D.L. (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland MA.

    Van Peenen, P.F.D., Cunningham, M.L. & Duncan, J.F. (1970) A collection of mammals from Con Son Island, Vietnam. Journal of Mammalogy, 51, 419–424.