Russian Journal of Genetics

, Volume 47, Issue 2, pp 205–215 | Cite as

Genetic diversity and phylogenetic relationships in the zokor subfamily myospalacinae (Rodentia, Muridae) inferred from RAPD-PCR

  • M. V. TsvirkaEmail author
  • M. V. Pavlenko
  • V. P. Korablev
Animal Genetics


Zokors (Myospalacinae) is a group of rodents specialized for underground life, endemics of eastern Asia, which is taxonomically and evolutionarily poorly studied. We examined genetic diversity and phylogenetic relationships among zokors (Myospalax myospalax, Myospalax aspalax, Myospalax armandii, Myospalax psilurus, Myospalax smithii) using RAPD-PCR. The subfamily Myospalacinae was shown to be monophyletic and contain four evolutionary branches: M. myospalax, M. aspalax-M. armandii, M. smithii and M. psilurus. Genetic differences and high differentiation were found among the species and between two geographic forms of Manchurian zokor M. psilurus from the marginal parts of the range, Transbaikalia and Primorye. The psiluris phylogroup was shown to be dichotomically divided into two clades according to the geographical distribution of animals from Transbaikalia and Primorye. The genetic differentiation between the geographic forms of M. psilurus corresponded to the differentiation between morphologically similar species M. aspalax and M. armandii. M. armandii is a sister taxon with regard to M. aspalax. This new evidence on the evolutionary relationships among zokors does not contradict the traditional views inferred from morphological, karyological, and allozyme data, on apartness of M. myospalax and the character of evolution in this group. The species status of Myospalax psilurus Milne-Edwards, 1874, M. epsilanus Thomas, 1912, and M. armandii Milne-Edwards, 1867, which had been suggested earlier on the basis of biochemical and karyological data, was confirmed.


Genetic Differentiation Ground Squirrel Genetic Variation Parameter Total Gene Diversity Arctic Ground Squirrel 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Lawrence, M.A., A Fossil Myospalax Cranium (Rodentia, Muridae) from Shanxi, China, with Observations on Zokor Relationships, Bull. Am. Mus. Nat. History, Griffiths, T.A. and Klingener, D., Eds., 1991, vol. 206, pp. 261–286.Google Scholar
  2. 2.
    Norris, R.W., Zhou, K.Y., Zhou, C.Q., et al., The Phylogenetic Position of the Zokors (Myospalacinae) and Comments on the Families of Muroids (Rodentia), Mol. Phyl. Evol., 2004, vol. 31, pp. 972–978.CrossRefGoogle Scholar
  3. 3.
    Jansa, S.A. and Weksler, M., Phylogeny of Muroid Rodents: Relationships within and among Major Lineages as Determined by IRBP Gene Sequences, Mol. Phyl. Evol., 2004, vol. 31, pp. 256–276.CrossRefGoogle Scholar
  4. 4.
    Fan, N.C. and Shi, Y.Z., A Revision of the Zokors of Subgenus Eospalax, Acta Theriol. Sin., 1982, vol. 2, no. 2, pp. 183–197.Google Scholar
  5. 5.
    Musser, G.G and Carleton, M.D., Family Muridae, Mammal Species of the World: A Taxonomic and Geographic Reference, Wilson, D.E. and Reeder, D.M., Eds., Washington: Smiths., 1993, pp. 501–756.Google Scholar
  6. 6.
    Zheng, S.H, Classification and Evolution of the Siphneidae, Rodent and Lagomorph Families of Asian Origins and Diversification, Tomida, Y., Li, C.-K., and Setoguchi, T., Eds., vol. 8 of National Science Museum Monographs, 1994, pp. 57–76.Google Scholar
  7. 7.
    Zhou, C. and Zhou, K., The Validity of Different Zokor Species and the Genus Eospalax Inferred from Mitochondrial Gene Sequences, Integrative Zool., 2008, vol. 3, pp. 290–298.CrossRefGoogle Scholar
  8. 8.
    Puzachenko, A.Yu., Pavlenko, M.V., and Korablev, V.P., Morphometric Craniological Variability of the Zokors (Myospalacinae, Rodentia), Zool. Zh., 2009, vol. 88, no. 1, pp. 92–112.Google Scholar
  9. 9.
    Pavlinov, I.Ya., Yakhontov, E.L., and Agadzhanyan, A.K., Mlekopitayushchie Evrazii: 1. Rodentia: sistematikogeograficheskii spravochnik. (Eurasian Mammals: 1. Rodentia: Taxonomic and Geographic Guide), Rossolimo, O.L., Ed., Moscow: Mosk. Gos. Univ., 1995.Google Scholar
  10. 10.
    Distribution of Mammalian Species in China, Zhang, Y., et al., Eds., China Forestry Pub. House, 1997.Google Scholar
  11. 11.
    Corbet, G.B., The Mammals of the Palearctic Region: A Taxonomic Review, London: Cornell Univ. Press, 1978.Google Scholar
  12. 12.
    Lyapunova, E.A., Vorontsov, N.N., and Martynova, L.Ya., Cytogenetical Differentiation of Burrowing Mammals in Palaearctis, in Symposium Theriologisum: 2. Proceedings of International Symposium on Species and Zoogeography of European Mammals, Praha: Academia, 1974, pp. 203–215.Google Scholar
  13. 13.
    Martynova L.Ya., Vorontsov N.N. Population Cytogenetics of Zokors (Myospalacinae, Rodentia), in Sistematika i tsitogenetika mlekopitayushchikh (Systematics and Cytogenetics of Mammals), Moscow: Nauka, 1975, pp. 13–15.Google Scholar
  14. 14.
    Martynova, L.Ya., Chromosomal Differentiation of Three Species of Zokors (Rodentia, Myospalacinae), Zool. Zh., 1976, vol. 55, no. 8, pp. 1265–1268.Google Scholar
  15. 15.
    Korablev, V.P. and Pavlenko, M.V., Genetic Characteristics and Geographic Distribution of Zokors Myospalax (Rodentia) in South Transbaikalia, Prirodookhrannoe sotrudnichestvo Chitinskoi oblasti (Rossiiskaya Federatsiya) i avtonomnogo raiona Vnutrennyaya Mongoliya (KNR) v transgranichnykh ekologicheskikh regionakh (Environmental Cooperation between Chita Oblast (Russian Federation) and Inner Mongolia Autonomous Region (People Republic of China) in Transboundary Ecological Regions), Proc. Int. Conf., Chita, 2007, pp. 188–190.Google Scholar
  16. 16.
    Martynova, L.Ya., Fomicheva, I.I., and Vorontsov, N.N., An Electrophoretic Study of Blood Proteins in Three Species of Zokors (Rodentia, Myospalacinae), Zool. Zh., 1977, vol. 56, no. 10, pp. 1538–1542.Google Scholar
  17. 17.
    Pavlenko, M.V. and Korablev, V.P., Genetic Differentiation, Systematic Position, and the Problem of Conservation of the Transbaikal Zokor Myospalax psilurus (Rodentia, Myospalacinae) Marginal Populations, in Problemy evolyutsii (Problems of Evolution), Vladivostok: Dal’nauka, 2003, vol. 5, pp. 167–177.Google Scholar
  18. 18.
    Pavlenko, M.V. and Korablev, V.P., Genetic Diversity and Geographic Distribution of Zokors Myospalax (Rodentia) in South Transbaikalia, Ekosistemy Mongolii i prigranichnykh territorii sosednikh stran: Prirodnye resursy, bioraznoobrazie i ekologicheskie perspektivy (Ecosystems of Mongolia and Natural Territories of Neighboring Countries: Natural Resources, Biodiversity, and Ecological Perspectives), Proc. Int. Conf., Ulaan-Baatar, 2005, pp. 300–302.Google Scholar
  19. 19.
    Puzachenko, A., Pavlenko, M., and Korablev, V., Craniological Variability of the Zokors (Myospalacinae) with Simplified First Upper Molar, in Rodents et Spatium on Rodent Biology, Proc. 11th Int. Conf., Myshkin, 2008, p. 144.Google Scholar
  20. 20.
    Atopkin, D.M., Bogdanov, A.S., and Chelomina, G.N., Genetic Variation and Differentiation in Striped Field Mouse Apodemus agrarius Inferred from RAPD-PCR Analysis, Russ. J. Genet., 2007, vol. 43, no. 6, pp. 665–676.CrossRefGoogle Scholar
  21. 21.
    Lavrenchenko, L.A., Verheyen, E., and Potapov, S.G., et al., Divergent and Reticulate Processes in Evolution of Ethiopian Lophuromys flavopunctatus Species Complex: Evidence from Mitochondrial and Nuclear DNA Differentiation Patterns, Biol. J. Linnean Soc., 2004, vol. 83, pp. 301–316.CrossRefGoogle Scholar
  22. 22.
    Tsvirka, M.V., Genetic Diversity, Phylogenetic Relationships and Systematics of Palearctic Ground Squirrels of the Genus Spermophilus (Subgenera Citellus and Colobotis), Extended Abstract of Cand. Sci. (Biol.) Dissertation, Vladivostok: Institute of Biology and Soil Science, Far Eastern Branch of Russian Academy of Sciences, 2005, p. 24.Google Scholar
  23. 23.
    Tsvirka, M.V., Chelomina, G.N., and Korablev, V.P., Genetic Differentiation, Phylogenetics and Systematics of Desert Ground Squirrels of the Subgenus Colobotis (Spermophilus: Rodentia, Sciuridae), Zool. Zh., 2006, vol. 86, no. 5, pp. 629–640.Google Scholar
  24. 24.
    Tsvirka, M.V., Chelomina, G.N., and Korablev, V.P., Genetic Differentiation between two Palaearctic Groups of Ground-Squirrels, Subgenera Citellus and Colobotis (Spermophilus, Sciuridae, Rodentia), Based on RAPD-PCR Assay, in Proceedings of 1st European Ground Squirrel Meeting, Felsötárkány, 2006, p. 56.Google Scholar
  25. 25.
    Tatonova, Yu.V., Spiridonova, L.N., Tsvirka, M.V., and Korablev, V.P., Molecular-Genetic Relationship of Some Ground Squirrel Species of Genus Spermophilus (Sciuridae, Rodentia), Proceedings of 1st European Ground Squirrel Meeting, Felsötárkány, 2006, p. 54.Google Scholar
  26. 26.
    Tsvirka, M.V., Spiridonova, L.N., and Korablev, V.P., Molecular Genetic Relationships among East Palaearctic Ground Squirrels of the Genus Spermophilus (Sciuridae, Rodentia), Russ. J. Genet., 2008, vol. 44, no. 8, pp. 966–976.CrossRefGoogle Scholar
  27. 27.
    Ognev, S.I., Zveri SSSR i prilezhashchikh stran: Gryzuny (Animals of the Soviet Union and Neighboring Countries: Rodents), Moscow: Izd. Akad. Nauk SSSR, 1947, vol. 5, pp. 641–686.Google Scholar
  28. 28.
    Qing Ling, Meng Xiang-Ming, Kryukov, A., et al., Species and Distribution Patterns of Small Mammals in the Pingheliang Nature Reserve of Qinling Mountains, Shaanxi, Zool. Res., 2007, vol. 28, no. 3, pp. 231–242.Google Scholar
  29. 29.
    Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, New York: Cold Spring Harbor Lab., 1989.Google Scholar
  30. 30.
    Aljanabi, S.M. and Martinez, I., Universal and Rapid Salt-Extraction of High Quality Genomic DNA for PCR-Based Techniques, Nucleic Acids Res., 1997, vol. 25, no. 22, pp. 4692–4693.CrossRefPubMedGoogle Scholar
  31. 31.
    Tsvirka, M.V., Chelomina, G.N., and Korablev, V.P., Genetic Evidence for Hybridization between Paletailed Spermophilus pallidicauda Satunin, 1903 and Alashanic S. alaschanicus Büchner, 1888 Ground Squirrels in Mongolia, Russ. J. Genet., 2006, vol. 42, no. 4, pp. 421–428.CrossRefGoogle Scholar
  32. 32.
    Miller, M.P., Tools for Population Genetic Analysis (TFPGA) 1.3: A Windows Program for the Analysis of Allozyme and Molecular Population Genetic Data, 1997, Computer Software Distributed by Author.Google Scholar
  33. 33.
    Yeh, F.C. and Boyle, T.J.B., Population Genetic Analysis of Co-Dominant and Dominant Markers and Quantitative Traits, Belgian J. Botany, 1997, vol. 129, p. 159.Google Scholar
  34. 34.
    Van de Peer, Y. and De Wacher, R., TREECON for Windows: A Software Package for the Construction and Drawing of Evolutionary Trees for the Microsoft Windows Environment, Comput. Applic. Biosci., 1994, vol. 10, pp. 569–570.Google Scholar
  35. 35.
    Pavlenko, M., Korablev, V., Tsvirka, M., et al., Genetic Differentiation of Zokors (Rodentia, Myospalacinae) from East Russia: Protein Electrophoretic Markers, Karyological and Molecular Data, in Rodents et Spatium on Rodent Biology, Proc. 11th Int. Conf., Myshkin, 2008, p. 57.Google Scholar
  36. 36.
    Tsvirka, M.V., Pavlenko, M.V., and Korablev, V.P., Genetic Differentiation and Phylogenetic Relations of Zokors (Rodentia, Myospalacinae) Inferred from Molecular-Genetic Analysis, in Proceedings of 5th Meeting of All-Russian Society of Geneticists and Breeders, Moscow: Ross. Gos. Agrarnyi Univ.-Mosk. S-kh. Akad., 2009.Google Scholar
  37. 37.
    Tsvirka, M., Pavlenko, M., Korablev, V., et al., Molecular-Genetic Relationships of the Zokors (Rodentia, Myospalacinae): Analysis of D-Loop Region Polymorphism, in Modern Achievements in Population, Evolutionary, and Ecological Genetics, Proc. Int. Symp., Vladivostok: Vostok Marine Biological Station, 2009, pp. 6–12.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • M. V. Tsvirka
    • 1
    Email author
  • M. V. Pavlenko
    • 1
  • V. P. Korablev
    • 1
  1. 1.Institute of Biology and Soil Sciences, Far Eastern BranchRussian Academy of SciencesVladivostokRussia

Personalised recommendations