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Phylogeography of the Common Vole Microtus arvalis, the Obscurus Form (Rodentia, Arvicolinae): New Data on the Mitochondrial DNA Variability

Abstract

Genetic diversity of the common vole Microtus arvalis Pall., 1778 of the obscurus form was examined by analyzing the variability of two markers, the cytochrome b gene (1143 bp) and the fragment of the mitochondrial DNA control region (800 bp). One hundred forty-five individuals were captured at 39 locations from the Crimean Peninsula in the west to northern Altai in the east. On the basis of the analysis of the cytochrome b gene sequences, all M. arvalis individuals of the obscurus form from the regions under consideration were assigned to the previously identified Sino-Russian clade, distributed in the main part of the range of the obscurus form. On the basis of concatenated sequences of the two mtDNA markers, the internal structure of the Sino-Russian clade was established and two subclades, Crimean and Eurasian, were identified. In the Eurasian subclade, related haplotypes form several geographically localized groups (Vyatka–Ural, Volga–Ural, Southern Ural, Southern Cis-Urals 1, and Southern Cis-Urals 2). The groups are connected with each other through a widespread set of poorly differentiated haplotypes found from the Cis-Urals to Western Siberia. Two haplotypes from the North Altai and northern foothills of the Altai Mountains are included in the Eurasian subclade. However, these haplotypes are separated from each other and from haplotypes of other groups by distances comparable with the intergroup distance for this subclade. Demographic analysis enables the conclusion that the history of the Sino-Russian clade of M. arvalis of the form obscurus has regional specificity. Haplotypes found in seven locations on the Crimean Peninsula are most likely the result of a single expansion event, whereas for the Eurasian subclade, several successive waves of expansion can be proposed.

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REFERENCES

  1. Malygin, V.M., Sistematika obyknovennykh polevok (Systematics of Common Voles), Moscow: Nauka, 1983.

    Google Scholar 

  2. Meier, M.N., Golenishchev, F.N., Radzhabli, S.I., and Sablina, O.L., Serye polevki fauny Rossii i sopredel’nykh territorii (Gray Voles of the Fauna of Russia and Adjacent Territories), in Tr. Zool. Inst. Ross. Akad. Nauk, 1996, vol. 232.

  3. Meier, M.N., Orlov, V.M., and Skholl’, E.D., Sibling species in the Microtus arvalis (Rodentia, Cricetidae) group, Zool. Zh., 1972, vol. 51, pp. 724-738.

    Google Scholar 

  4. Mammal Species of the World: A Taxonomic and Geographic Reference, Wilson, D.E. and Reeder, D.A.M., Eds., JHU Press, 2005.

    Google Scholar 

  5. Abramson, N.I. and Lisovskii, A.A., Subfamily Arvicolinae, Mlekopitayushchie Rossii: sistematiko-geograficheskii spravochnik (Mammals of Russia: A Systematic and Geographical Reference Book), vol. 52 of Trudy Zoologicheskogo muzeya Moskovskogo gosudarstvennogo universiteta (Proceedings of Zoological Museum of the Moscow State University), 2012, pp. 127-141.

  6. Lavrenchenko, L.A., Potapov, S.G., Bulatova, N.Sh., and Golenishchev, F.N., A genetic study of natural hybridization between two forms of the common vole (Microtus arvalis) with the use of molecular and cytogenetic methods, Dokl. Biol. Sci., 2009, vol. 426, nos. 1-6, pp. 222-224.

    Article  PubMed  CAS  Google Scholar 

  7. Malygin, V.M., Morphological criteria for determining of holotypes of species taxa of common voles (Microtus, Rodentia, Mammalia), Dokl. Biol. Sci., 1996, vol. 346, no. 2, pp. 282-286.

    Google Scholar 

  8. Tougard, C., Montuire, S., Volobouev, V., et al., Exploring phylogeography and species limits in the Altai vole (Rodentia: Cricetidae), Biol. J. Linn. Soc., 2013, vol. 108, no. 2, pp. 434-452.

    Article  Google Scholar 

  9. Haynes, S., Jaarola, M., and Searle, J.B., Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago, Mol. Ecol., 2003, vol. 12, no. 4, pp. 951-956.

    Article  PubMed  CAS  Google Scholar 

  10. Tougard, C., Renvoise, E., Petitjean, A., and Quere, J.P., New insight into the colonization processes of common voles: inferences from molecular and fossil evidence, PLoS One, 2008, vol. 3, no. 10. e3532

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Bužan, E.V., Förster, D.W., Searle, J.B., and Kryštufek, B., A new cytochrome b phylogroup of the common vole (Microtus arvalis) endemic to the Balkans and its implications for the evolutionary history of the species, Biol. J. Linn. Soc., 2010, vol. 100, no. 4, pp. 788-796.

    Article  Google Scholar 

  12. Bulatova, N.Sh., Potapov, S.G., and Lavrenchenko, L.A., Genomic versus chromosomal polytypy in studies of mitochondrial and nuclear DNA markers in the Microtus arvalis group, Russ. J. Genet., 2010, vol. 46, no. 5, pp. 586-594. https://doi.org/10.1134/ S1022795410050121.

    Article  CAS  Google Scholar 

  13. Gromov, A.R., Bulatova, N.Sh., Potapov, S.G., et al., Study of the hybridization zone of 46-chromosome forms of voles in the Vladimirskaya oblast, Struktura vida u mlekopitayushchikh (Species Structure in Mammals) (Proc. Conf.), Moscow: KMK, 2010, p. 29.

  14. Fink, S., Excoffier, L., and Heckel, G., Mitochondrial gene diversity in the common vole Microtus arvalis shaped by historical divergence and local adaptations, Mol. Ecol., 2004, vol. 13, pp. 3501-3514.

    Article  PubMed  CAS  Google Scholar 

  15. Stojak, J., McDevitt, A.D., Herman, J.S., et al., Post-glacial colonization of eastern Europe from the Carpathian refugium: evidence from mitochondrial DNA of the common vole Microtus arvalis, Biol. J. Linn. Soc., 2015, vol. 115, no. 4, pp. 927-939.

    Article  Google Scholar 

  16. Stojak, J., McDevitt, A.D., Herman, J.S., et al., Between the Balkans and the Baltic: phylogeography of a common vole mitochondrial DNA lineage limited to Central Europe, PLoS One, 2016, vol. 11, no. 12. e0168621

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Mahmoudi, A., Darvish, J., Aliabadian, M., et al., New insight into the cradle of the grey voles (subgenus Microtus) inferred from mitochondrial cytochrome b sequences, Mammalia, 2017, vol. 81, no. 6, pp. 583-593.

    Article  Google Scholar 

  18. Irwin, D.M., Kocher, T.D., and Wilson, A.C., Evolution of the cytochrome b gene of mammals, J. Mol. Evol., 1991, vol. 32, no. 2, pp. 128-144.

    Article  PubMed  CAS  Google Scholar 

  19. Clayton, D.A., Transcription and replication of animal mitochondrial DNAs, Int. Rev. Cytol., 1992, vol. 141, pp. 217-232.

    Article  PubMed  CAS  Google Scholar 

  20. Nekrutenko, A., Makova, K.D., Chesser, R.K., and Baker, R.J., Representational difference analysis to distinguish cryptic species, Mol. Ecol., 1999, vol. 8, no. 7, pp. 1235-1237.

    Article  PubMed  CAS  Google Scholar 

  21. Zhumabekova, B.K., Issakaev, Y.M., Surov, A.V., et al., INSDC (GenBank). https://www.ncbi.nlm.nih. gov/nuccore/?term=Microtus +obscurus + Zhumabekova. Accessed November 11, 2013.

  22. Tkachenko, E.A., Witkowski, P.T., Radosa, L., et al., Adler hantavirus, a new genetic variant of Tula virus identified in Major’s pine voles (Microtus majori) sampled in southern European Russia, Infect., Genet. Evol., 2015, vol. 29, pp. 156-163.

    Article  Google Scholar 

  23. Triant, D.A. and DeWoody, J.A., Accelerated molecular evolution in Microtus (Rodentia) as assessed via complete mitochondrial genome sequences, Genetica, 2006, vol. 128, no. 1, pp. 95-108.

    Article  PubMed  CAS  Google Scholar 

  24. Jaarola, M., Martínková, N., Gündüz, I., et al., Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences, Mol. Phylogenet. Evol., 2004, vol. 33, pp. 647-663.

    Article  PubMed  CAS  Google Scholar 

  25. Shenbrot, G.I. and Krasnov, B.R., An Atlas of the Geographic Distribution of the Arvicoline Rodents of the World (Rodentia, Muridae: Arvicolinae), Sofia: Pensoft, 2005.

    Google Scholar 

  26. Zagorodnyuk, I.V., Taxonomy and the distribution of Ukrainian gray voles (Rodentiformes: Arvicolini), in Mlekopitayushchie Ukrainy (Mammals of Ukraina), Kiev: Naukova Dumka, 1993, pp. 63-76.

    Google Scholar 

  27. Markova, E.A., Yalkovskaya, L.E., and Zykov, S.V., Taxonomic identity of voles of the “arvalis” group (genus Microtus, Arvicolinae, Rodentia) at the northern boundary of their distribution in the Urals, Dokl. Biol. Sci., 2010, vol. 432, nos. 1-6, pp. 212-215.

    Article  PubMed  CAS  Google Scholar 

  28. Demirsoy, A., Rodents of Türkiye: Türkiye Kemiricileri, Ankara: Meteksan, 2006.

    Google Scholar 

  29. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Sibiryakov, P.A. and Amerkhanova, L.I., Assessment of the quality of DNA preservation in museum specimens of animal tissues, Ekologiya: fakty, gipotezy, modeli (Ecology: Facts, Hypotheses, Models) (Proc. Conf. Young Sci.), Yekaterinburg: Goshitskii, 2016, pp. 108-109.

  31. Tougard, C., Delefosse, T., Hänni, C., and Montgelard, C., Phylogenetic relationships of the five extant rhinoceros species (Rhinocerotidae, Perissodactyla) based on mitochondrial cytochrome b and 12S rRNA genes, Mol. Phylogenet. Evol., 2001, vol. 19, no. 1, pp. 34-44.

    Article  PubMed  CAS  Google Scholar 

  32. Haring, E., Herzig Straschil, B., and Spitzenberger, F., Phylogenetic analysis of Alpine voles of the Microtus multiplex complex using the mitochondrial control region, J. Zool. System. Evol. Res., 2000, vol. 38, no. 4, pp. 231-238.

    Article  Google Scholar 

  33. Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT, Nucleic Acids Symp. Ser., 1999, vol. 41, pp. 95-98.

    CAS  Google Scholar 

  34. Tamura, K., Stecher, G., Peterson, D., et al., MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725-2729. doi 10.1093/molbev/mst197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Ronquist, F. and Huelsenbeck, J.P., MrBayes 3: Bayesian phylogenetic inference under mixed models, Bioinformatics, 2003, vol. 19, no. 12, pp. 1572-1574.

    Article  PubMed  CAS  Google Scholar 

  36. Nylander, J.A.A., MrModeltest, Version 2, Program distributed by the author, Uppsala: Evolutionary Biology Centre, Uppsala University, 2004, vol. 2.

    Google Scholar 

  37. Bandelt, H.-J., Forster, P., and Röhl, A., Median-joining networks for inferring intraspecific phylogenies, Mol. Biol. Evol., 1999, vol. 16, pp. 37-48.

    Article  PubMed  CAS  Google Scholar 

  38. Excoffier, L., Laval, G., and Schneider, S., Arlequin ver. 3.0: an integrated software package for population genetics data analysis, Evol. Bioinf. Online, 2005, vol. 1, pp. 47-50.

    CAS  Article  Google Scholar 

  39. Librado, P. and Rozas, J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 2009, vol. 25, pp. 1451-1452.

    Article  PubMed  CAS  Google Scholar 

  40. Farris, J.S., Källersjö, M., Kluge, A.G., and Bult, C., Testing significance of incongruence, Cladistics, 1995, vol. 10, no. 3, pp. 315-319.

    Article  Google Scholar 

  41. Swofford, D.L., PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods): Version 4.0b10, Sunderland: Sinauer Associates, 2002.

    Google Scholar 

  42. Tamura, K., Estimation of the number of nucleotide substitutions when there are strong transition—transversion and G + C-content biases, Mol. Biol. Evol., 1992, vol. 9, pp. 678-687.

    PubMed  CAS  Google Scholar 

  43. Tavaré, S., Some probabilistic and statistical problems in the analysis of DNA sequences: some mathematical questions in biology—DNA sequence analysis, Lect. Math. Life Sci., 1986, vol. 17, no. 2, pp. 57-86.

    Google Scholar 

  44. Kimura, M., A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol., 1980, vol. 16, no. 2, pp. 111-120.

    Article  PubMed  CAS  Google Scholar 

  45. Hasegawa, M., Kishino, K., and Yano, T., Dating the human—ape splitting by a molecular clock of mitochondrial DNA, J. Mol. Evol., 1985, vol. 22, no. 2, pp. 160-174.

    Article  PubMed  CAS  Google Scholar 

  46. Zvychainaya, E.Yu., Danilkin, A.A., Kholodova, M.V., et al., Analysis of the variability of the control region and cytochrome b gene of mtDNA of Capreolus pygargus Pall., Biol. Bull., 2011, vol. 38, article 1134. https://doi.org/10.1134/S1062359011050189.

    Article  CAS  Google Scholar 

  47. Abramson, N.I., Phylogeography: results, problems, perspectives, Vavilovskii Zh. Genet. Sel., 2007, vol. 11, no. 2, pp. 307-331.

    Google Scholar 

  48. Khrunyk, Yu.Ya., Bogdanov, V.D., Yalkovskaya, L.E., et al., The genetic diversity of burbot (Lota lota L., 1758) of Western Siberia (the analysis of the mtDNA control region polymorphism), Russ. J. Genet., 2017, vol. 53, no. 2, pp. 233-241. https://doi.org/10.1134/ S1022795417010082.

    Article  CAS  Google Scholar 

  49. Polityko, Yu.K. and Sibiryakov, P.A., Variability of mitochondrial DNA of Arctic char (Salvelinus alpinus L., 1758) from the Polar Urals, Ekologiya. Genetika. Evolutsiya (Ecology. Genetics. Evolution) (Proc. Conf. Young Sci.), Yekaterinburg: Goshitskii, 2015, pp. 122-128.

  50. Yigit, N., Hutterer, R., Krystufek, B., and Amori, G., Microtus arvalis, The IUCN Red List of Threatened Species, 2016. http://dx.doi.org/ 10.2305/IUCN.UK.2016-2.RLTS.T13488A22351133.en. Accessed Juni 10, 2016.

  51. Demidovich, A.P. and Lipin, S.I., Biology of common vole in the Irkutsk oblast, Vestn. Irkutsk Gos. S-kh. Akad., 1997, no. 3, pp. 1-25.

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ACKNOWLEDGMENTS

We thank Zoological museum of the institute of Plant and Animal Ecology, Ural Branch of Russian Academy of Sciences, Yekaterinburg and our collegs A.V. Borodin, T.V. Strukova, S.B. Rakitin, and D.A. Toporkova (Institute of Plant and Animal Ecology, Ural Branch of Russian Academy of Sciences, Yekaterinburg) for kindly providing collection specimens for the analysis and S.V. Zykov, M.A. Fominykh, L.I. Amerkhanova, E.V. Zinoviev, E.P. Izvarin, E.Yu. Zakharova, T.S. Oslina, A.O. Shkurikhin (Institute of Plant and Animal Ecology, Ural Branch of Russian Academy of Sciences, Ekaterinburg), and R.Yu. Dudko (Institute of Systematics and Ecology of Animals, Siberian Branch of Russian Academy of Sciences, Novosibirsk) for their help in organizing field studies and catching small mammals. Special thanks to the Joint Directorate of the Orenburg and Shaitan-Tau State Nature Reserves, personally to O.V. Soroka and inspectors of the Talovskaya Steppe, Aituirskaya Steppe, and Aschisay Steppe sites for assistance in organizing and carrying out small mammal catching in the Orenburg Reserve, and the Administration of the Buzuluksky Bor National Park for assistance in organizing catching on the territory of the national park. We also thank G.A. Tsaur and the staff of the Laboratory of Molecular Biology, Immunophenotyping, and Pathomorphology of the Children’s Oncology and Hematology Center, Regional Children Hospital No. 1 (Yekaterinburg) for the opportunity to use an ABI Prism 3130 genetic analyzer (Applied Biosystems, United States).

This study was supported by the Russian Foundation for Basic Research (grant no. 16-04-01486-a) and the Integrated Program of the Ural Branch of the Russian Academy of Sciences (grant no. 18-4-4-43).

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Sibiryakov, P.A., Tovpinets, N.N., Dupal, T.A. et al. Phylogeography of the Common Vole Microtus arvalis, the Obscurus Form (Rodentia, Arvicolinae): New Data on the Mitochondrial DNA Variability. Russ J Genet 54, 1185–1198 (2018). https://doi.org/10.1134/S1022795418100137

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Keywords:

  • Microtus arvalis
  • phylogeography
  • mitochondrial DNA
  • Crimea
  • Urals
  • Altai