Advertisement

Mammalian Biology

, Volume 76, Issue 3, pp 258–267 | Cite as

Phylogeny of Palearctic vole species (genus Microtus, Rodentia) based on mitochondrial sequences

  • Elisabeth HaringEmail author
  • Irina N. Sheremetyeva
  • Alexey P. Kryukov
Original Investigation

Abstract

Within the species-rich rodent genus Microtus, the Microtus fortis species-group is not well studied so far. We investigated DNA sequences of the mitochondrial control region in taxa of this group to assess the inter- and intraspecific variation and differentiation of populations, and to establish a molecular phylogeny. For comparison, samples of Microtus oeconomus covering the species distribution range were analyzed. Within the M. fortis group five distinct highly supported lineages were found. Four of them represent single species: Microtus fortis, Microtus sachalinensis, Microtus hyperboreus, and Microtus gromovi. The fifth clade comprises Microtus mujanensis, Microtus evoronensis and Microtus maximowiczii. Genetic distances between these five lineages range from 5.4% to 9.2%. The distinct position of M. gromovi confirms the proposed species status suggested by earlier chromosome and cranial-morphological investigations. The trees also indicate that M. hyperboreus belongs to the M. fortis group and is the sister group of M. gromovi. Genetic diversity is rather high within the East Asian M. fortis species-group, which is also characterized by high chromosomal variation as determined in previous studies. The phylogeographic relationships found in M. oeconomus are in accordance with previous findings based on the mitochondrial cytochrome b gene. There are tree main haplogroups (Europe, Siberia, Beringia) found in this Holarctic species. The genetic distances between these groups in the mitochondrial control region range from 3.4% to 4.1%.

In general, genetic diversity and species richness of voles in the Eastern Palearctic implies that this region might have provided ideal conditions for the radiation of this species group.

Keywords

Microtus fortis species-group Microtus oeconomus Mitochondrial control region Phylogeography 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abramson, N.I., Tikhonova, E.P., 2005. Reevaluation of taxonomic structure of the root vole (Microtus oeconomus Pallas, 1776, Rodentia, Arvicolidae) from the territory of the former USSR based on evidence of craniometric and molecular data. Russ. J. Theriol. 4, 63–73.CrossRefGoogle Scholar
  2. Allen, G.M., 1940. The mammals of China and Mongolia. Am. Mus. Nat. Hist., New York.Google Scholar
  3. Bannikova, A.A., Lebedev, V.S., Lissovsky, A.A., Matrosova, V., Abramson, N.I., Obolenskaya, E.V., Tesakov, A.S., 2010. Molecular phylogeny and evolution of the Asian lineage of vole genus Microtus (Rodentia: Arvicolinae) inferred from mitochondrial cytochrome b sequence. Biological Journal of the Linnean Society 99, 595–613.CrossRefGoogle Scholar
  4. Belyanin, A.N., Belyanina, V.N., Gavrilova, V.V., 1986. Karyotype properties of the root vole (Microtus oeconomus) from the different parts of the range. In: Abst. 4th meet. Russian Theriol. Soc. Nauka Publ., Moscow, pp. 44–45 (in Russian).Google Scholar
  5. Bininda-Emonds, O.R.P., 2007. Fast genes and slow clades: comparative rates of molecular evolution in mammals. Evolut. Bioinform. 3, 59–85.Google Scholar
  6. Bobrinsky, N.A., Kuznetsov, B.A., Kuzyakin, A.P., 1965. Check-list of the Mammals of the USSR. Prosveshchenie, Moscow (in Russian).Google Scholar
  7. Bogatov, V.V., Pietsch, Th.W., Storozhenko, S.Yu., Barkalov, V.Yu., Lelej, A.S., Kholin, S.K., Krestov, P.V., Kostenko, V.A., Makarchenko, E.A., Prozorova, L.A., Shedko, S.V., 2006. Origin patterns of the terrestrial and freshwater biota of Sakhalin Island. Bulletin of the Far Eastern Branch. Russ. Acad. Sci. 2, 32–47 (in Russian).Google Scholar
  8. Brunhoff, C., Galbreath, K.E., Fedorov, V.B., Cook, J.A., Jaarola, M., 2003. Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes. Mol. Ecol. 12, 957–968.PubMedCrossRefPubMedCentralGoogle Scholar
  9. Castiglia, R., Annesi, F., Aloise, G., Amori, G., 2008. Systematics of the Microtus savii complex (Rodentia, Cricetidae) via mitochondrial DNA analyses: Paraphyly and pattern of sex chromosome evolution. Mol. Phyl. Evol. 46, 1157–1164.CrossRefGoogle Scholar
  10. Chaline, J., Brunet-Lecomte, P., Montuire, S., Viriot, L., Courant, F., 1999. Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoecological history and evolutionary data. Ann. Zool. Fenn. 36, 239–267.Google Scholar
  11. Chaline, J., 1987. Arvicolid data (Arvicolidae, Rodentia) and evolutionary concepts. Evol. Biol. 21, 237–310.CrossRefGoogle Scholar
  12. Conroy, C.J., Cook, J.A., 2000. Molecular systematics of a holarctic rodent (Microtus: Muridae). J. Mammal 81, 344–359.CrossRefGoogle Scholar
  13. Dobson, M., 1994. Patterns of distribution in Japanese land mammals. Mammal Rev. 24, 91–111.CrossRefGoogle Scholar
  14. Ellerman, J.R., 1941. The Families and Genera of Living Rodents, vol. II. British Museum, London (Natural History).Google Scholar
  15. Ellerman, J.R., Morrison-Scott, T.C.S., 1951. Checklist of Palearctic and Indian Mammals 1758 to 1946. British Museum, London (Natural History).Google Scholar
  16. Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47–50.CrossRefGoogle Scholar
  17. Fink, S., Excoffier, L., Heckel, G., 2004. Mitochondrial gene diversity in the common vole Microtus arvalis shaped by historical divergence and local adaptations. Mol. Ecol. 13, 3501–3514.PubMedCrossRefPubMedCentralGoogle Scholar
  18. Fredga, K., Bergstrom, U., 1970. Chromosome polymorphism in the root vole (Microtus oeconomus). Hereditas 66, 145–152.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Fredga, K., Persson, A., Stenseth, N.C., 1980. Centric fission in Microtus oeconomus. A chromosome study of isolation in Fennoscandia. Hereditas 9, 209–216.Google Scholar
  20. Frisman, L.V., Korobitsyna, K.V., Kartavtseva, I.V., Sheremetyeva, I.N., Vouta, L.L., 2009. Voles (Microtus Shrank, 1798) of the Russian Far East: Allozymic and karyological divergence. Russ. J. Genet. 45, 707–714.CrossRefGoogle Scholar
  21. Frisman, L.V., Kartavtseva, I.V., Kostenko, V.A., Sheremetyeva, I.N., Chernyavskii, F.B., 2003. Genogeographic variability and genetic differentiation of the root vole (Microtus oeconomus Pallas, 1776, Cricetidae, Rodentia) from the Kuril Islands. Russ. J. Genet. 39, 1363–1372.CrossRefGoogle Scholar
  22. Galbreath, K.E., Cook, J.K., 2004. Genetic consequences of Pleistocene glaciations for the tundra vole (Microtus oeconomus) in Beringia. Mol. Ecol. 13, 135–148.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Galleni, L., Stanyon, R., Contadini, L., Tellini, A., 1998. Biological and karyological data of the Mictrotus savii group (Rodentia, Arvicolidae) in Italy. Bonn. Zool. Beitr. 47, 277–282.Google Scholar
  24. Golenishchev, F.N., Radjabli, S.I., 1981. New species of gray vole from shore of Evoron Lake. Doklady Acad. Sci. USSR 257, 248–250 (in Russian).Google Scholar
  25. Gromov, I.M., Polyakov, I.Ya., 1977. Voles (Microtinae). Fauna of the USSR. Mammals. V. 3. Is. 8. Nauka publ., Leningrad (in Russian).Google Scholar
  26. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95–98.Google Scholar
  27. Haring, E., Herzig-Straschil, B., Spitzenberger, F., 2000. Phylogenetic analysis of Alpine voles of the Microtus multiplex complex using the mitochondrial control region. J. Zool. Syst. Evol. Res. 38, 231–238.CrossRefGoogle Scholar
  28. Haring, E., Sheremetyeva, I.N., Kryukov, A.P., 2005. Molecular phylogeny and phylogeography of some Palearctic vole species (genus Microtus) based on mitochondrial sequences. Abstract. In: Ninth International Mammalogical Congress (IMC9), Sapporo, Japan, pp. 163–164.Google Scholar
  29. Hellborg, L., Gündüz, I., Jaarola, M., 2005. Analysis of sex-linked sequences supports a new mammal species in Europe. Mol. Ecol. 14, 2025–2031.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Huelsenbeck, J.P., Ronquist, F., 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.CrossRefPubMedGoogle Scholar
  31. Jaarola, M., Martínková, N., Gündüz, I., et al., 2004. Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol. Phylogenet. Evol. 33, 647–663.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Kartavtseva, I.V., Sheremetyeva, I.N., Korobitsina, K.V., Nemkova, G.A., Konovalova, E.V., Korablev, V.P., Voyta, L.L., 2008. Chromosomal forms of Microtus maximowiczii (Schrenck, 1858) (Rodentia, Cricetidae): variability in 2n and NF in different geographic regions. Russ. J. Theriol. 7, 89–97.CrossRefGoogle Scholar
  33. Korobitsyna, K.V., Kartavtseva, I.V., Frisman, L.V., Kryukov, A.P., Voyta, L.L., 2005. Chromosomal polymorphism and allozyme differentiation in vole Microtus maximowiczii Schrenk, 1858 from Transbaikalia region. In: Ecosystems of Mongolia and Frontier Areas of Adjacent Countries: Natural Resources, Biodiversity and Ecological Prospects. Publishing House Bembi San, Ulaanbaatar, pp. 287–289.Google Scholar
  34. Kostenko, V.A., 2000. Rodents (Rodentia) of the Far East of Russia. Dalnauka, Vladivostok (in Russian).Google Scholar
  35. Kostenko, V.A., Allenova, T.V., 1989. Intraspecies differentiation of the root vole in the Far East and distributional history of its subspecific form. In: Kostenko, V.A. (Ed.), Theriological Studies of the Southern Far East. Far East Div. Russian Acad. Sci., Vladivostok, pp. 4–25 (in Russian).Google Scholar
  36. Kovalskaya, Yu.M., 1977. Chromosome polymorphism in Microtus maximowiczii Schrenk, 1858 (Rodentia, Cricetidae). Bull. Moscow Soc. Nat. Investig. 82, 38–48 (in Russian, with English summary).Google Scholar
  37. Kovalskaya, Yu.M., Aniskin, V.M., Kartavtseva, I.V., 1991. Geographic variation relative to C heterochromatin in Microtus fortis (Rodentia, Cricetidae). Zoologicheskii Zhurnal 70, 97–103 (in Russian, with English summary).Google Scholar
  38. Kovalskaya, Yu.M., Sokolov, V.E., 1980. The new species of voles (Rodentia, Cricetidae, Microtinae) from low Priamurye. Zoologicheskii Zhurnal 59, 1409–1416.Google Scholar
  39. Kovalskaya, Yu.M., Khotolkhu, N., Orlov, V.N., 1980. Geographical distribution of chromosome mutations and structure of the species Microtus maximowiczii (Rodentia, Cricetidae). Zoologicheskii Zhurnal 59, 1862–1869 (in Russian, with English summary).Google Scholar
  40. Kozlovskii, A.N., Khvorostyanskaya, L.P., 1978. Stability of chromosome numbers in some species of rodents of the North-Eastern Siberia. In: Kontrimavichus, V.L. (Ed.), Fauna and Zoogeography of Mammals of the North-Eastern Siberia. Far East Sci. Center Russian Acad. Sci., Vladivostok, pp. 106–119 (in Russian).Google Scholar
  41. Kral, B., 1972. Chromosome characteristics of Muridea and Microtidae from Czechoslovakia. Acta Sci. Nat. Acad. Sci. Bohemoslovacae, Brno, 1–73.Google Scholar
  42. Kumar, S., 1996. PHYLTEST: A Program for Testing Phylogenetic Hypotheses. Version 2.0. Pennsylvania State University, Institute of Molecular Evolutionary Genetics and Department of Biology, University Park, PA.Google Scholar
  43. Kumar, S., Tamura, K., Nei, M., 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5, 150–163.PubMedCrossRefPubMedCentralGoogle Scholar
  44. Kumar, S., Subramanian, S., 2002. Mutation rates in mammalian genomes. Proc. Natl. Acad. Sci. U.S.A. 99, 803–808.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kumar, S., 2005. Molecular clocks: four decades of evolution. Nat. Rev. Genet. 6, 654–662.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Makino, S., 1950. Studies of murine chromosomes. VI. Morphology of the sex chromosomes in two species of Microtus. Annot. Zool. Japan 23, 63–68.Google Scholar
  47. Martin, A.P., Palumbi, S.R., 1993. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl. Acad. Sci. U.S.A. 90, 4087–4091.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Martínková, N., Zima, J., Jaarola, M., Macholán, M., Spitzenberger, F., 2007. The origin and phylogenetic relationships of Microtus bavaricus based on karyotype and mitochondrial DNA sequences. Folia Zool. 56 (1), 39–49.Google Scholar
  49. Maruyama, T., Imai, H.T., 1981. Evolutionary rate of the mammalian karyotype. J. Theor. Biol. 90, 111–121.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Matthey, R., 1954. Nouvelles recherches sur les chromosomes des Muridae. Caryologia 6, 1–44.CrossRefGoogle Scholar
  51. Meyer, M.N., Golenishchev, F.N., Radjably, S.I., Sablina, O.V., 1996. Voles (subgenus Microtus Schrank) of Russia and adjacent territories. Zool. Inst. Russian Acad. Sci., Sankt-Petersburg (in Russian).Google Scholar
  52. Mitsainas, G.P., Rovatsos, M.T., Giagia-Athanasopoulou, E.B., 2008. Heterochromatin study and geographical distribution of Microtus species (Rodentia, Arvicolinae) from Greece. Mammalian Biology—Zeitschrift fur Saugetierkunde 75, 261–269.CrossRefGoogle Scholar
  53. Millien-Parra, V., Jaeger, J.-J., 1999. Island biogeography of the Japanese terrestrial mammal assemblages: an example of a relict fauna. Biogeography 26, 959–972.CrossRefGoogle Scholar
  54. Ognev, S.I., 1950. Animals of the Soviet Union and the Neighboring Countries: Rodents. V. 7. Gosizdat, Moscow-Leningrad (in Russian).Google Scholar
  55. Orlov, V.N., Kovalskaya, Yu.M., 1978. Microtus mujanensis sp. n. (Rodentia, Cricetidae) from the Vitim river basin. Zoologicheskii Zhurnal 18, 1224–1232 (in Russian, with English summary).Google Scholar
  56. Pavlinov, I.Y., Rossolimo, O.L., 1987. Systematics of the USSR Mammals. Moscow State Univ. Publ., Moscow.Google Scholar
  57. Posada, D., Crandall, K.A., 1998. Modeltest: Testing the model of DNA substitution. Bioinformatics 14, 817–818.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Pyastolova, O.A., 1971. Root vole. Trans. Inst. Plant and Animal Ecology, Sverdlovsk, 80, pp. 127–149.Google Scholar
  59. Raush, R.L., Raush, V.R., 1968. On the biology and systematic position of Microtus abbreviatis Miller, vole endemic to the St. Mattew Islands, Bering Sea. Zeitschr, Säugetierkunde, 33, pp. 65–99.Google Scholar
  60. Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstruction of phylogenetic trees. Mol. Biol. Evol. 4, 406–425.PubMedPubMedCentralGoogle Scholar
  61. Sheremetyeva, I., Kartavtseva, I., Haring, E., Frisman, L., Kryukov, A.P., 2008. Morphological and genetic characteristics of Microtus maximowiczii gromovi Vorontsov, Boeskorov, Lyapunova et Revin. In: 1988//11th International Conference Rodens et Spatium—on Rodent Biology, Myshkin, Russia, pp. 84.Google Scholar
  62. Sheremetyeva, I.N., Kartavtseva, I.V., Voyta, L.L., Kryukov, A.P., Haring, E., 2009. Morphometric analysis of intraspecific variation in Microtus maximowiczii (Rodentia, Cricetidae) in relation to chromosomal differentiation with reinstatement of Microtus gromovi Vorontsov, Boeskorov, Lyapunova et Revin, 1988, stat. nov. J. Zool. Syst. Evol. Res. 47, 42–48.CrossRefGoogle Scholar
  63. Swofford, D.L., 2002. PAUP *—Phylogenetic Analysis Using Parsimony (*and other methods). Vers. 4.0b6-10. Sinauer, Sunderland, MA.Google Scholar
  64. Tougard, C., Renvoise, E., Petitjean, A., Quéré, J.-P., 2008. New insight into the colonization processes of common voles: inferences from molecular and fossil evidence. PLoS One 3 (10), e3532, doi: https://doi.org/10.1371/journal.pone.0003532.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Triant, D.A., Dewoody, J.A., 2006. Accelerated molecular evolution in Microtus (Rodentia) as assessed via complete mitochondrial genome sequences. Genetica 128, 95–108.PubMedCrossRefPubMedCentralGoogle Scholar
  66. Tryfonopoulos, G., Thanou, E., Chondropoulos, B., Fraguedakis-Fsolis, S., 2008. mtDNA analysis reveals the ongoing speciation on Greek populations of Microtus (Terricola) thomasi (Arvicolidae, Rodentia). Biol. J. Linn. Soc. 95, 117–130.CrossRefGoogle Scholar
  67. Tvrtković, N., Pavlinić, I., Podnar, M. Microtus bavaricus discovered in Croatia: Southern refugium or geographical variation? Mammalian Biology—Zeitschrift fur Saugetierkunde, doi: 10.1016/j.mambio.200907001.Google Scholar
  68. Vorontsov, N.N., Lyapunova, E.A., Boeskorov, G.G., Revin, Y.V., 1986. Stability of the root vole (Microtus oeconomus) karyotype in the central part of its range and the history of formation of the species present range. Zoologicheskii Zhurnal 65, 1705–1715 (in Russian, with English summary).Google Scholar
  69. Vorontsov, N.N., Boeskorov, G.G., Lyapunova, E.A., Revin, Y.V., 1988. A new chromosome form and variability of molars in voles Microtus maximowiczii (Rodentia, Cricetidae). Zoologicheskii Zhurnal 67, 205–215.Google Scholar
  70. Vinogradov, B.S., Gromov, I.M., 1952. Rodents of the USSR fauna. USSR Acad Sci. Publ., Moscow, Leningrad (in Russian).Google Scholar
  71. Zagorodnyuk, I.V., 1990. Karyotype variation and systematics of the grey voles (Rodentia, Arvicolini). 1. Species composition and chromosome numbers. Vestnik Zoologii 2, 26–37 (in Russian).Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2010

Authors and Affiliations

  • Elisabeth Haring
    • 1
    Email author
  • Irina N. Sheremetyeva
    • 2
  • Alexey P. Kryukov
    • 2
  1. 1.Museum of Natural History ViennaViennaAustria
  2. 2.Institute of Biology and Soil ScienceRussian Academy of SciencesVladivostokRussia

Personalised recommendations