Skip to main content
SpringerLink
Log in

Genetic Variability of Three Isolated Populations of the Muya Valley Vole Alexandromys mujanensis Orlov et Kovalskaja, 1978 (Rodentia, Arvicolinae)

  • ANIMAL GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

In the present study, on the basis of cytogenetic and molecular genetic (mtDNA control region) analysis, genetic variability of the Muya valley vole, Alexandromys mujanensis, an endemic of Buryatia and the northwest of Zabaykalsky krai, was assessed. Three isolated valley vole populations from the Muisko-Kuandinskaya and Barguzinskaya depressions, as well as the Baunt Lake valley, were examined. Polymorphism in the number of autosomal arms (NFa = 46–49) with a stable number of chromosomes (2n = 38), determined by morphological variability of four pairs of autosomes (MMUJ2, MMUJ7, MMUJ8, and MMUJ14), rather than two, as previously thought, was revealed. To date, for the Muya valley vole, ten karyotype variants have been identified. It seems likely that chromosomal rearrangements (pericentric inversions, as well as two variants of fusion of acrocentric chromosome pairs, i.e., centromeric-centromeric and centromeric-telomeric), which led to variability in autosome morphology in the populations of the Muya valley vole, are not harmful. Analysis of the mtDNA control region revealed high haplotype and nucleotide diversity for the species as a whole, while in the valley vole samples from the Dzherginsky Nature Reserve (Barguzinskaya Depression) and the Baunt lake valley, nucleotide diversity was reduced compared to the sample from the Muisko-Kuandinskaya Depression. Despite the fact that each of the studied populations has a unique composition of chromosomal rearrangements and mtDNA haplotypes, higher similarity between the populations of the Muisko-Kuandinskaya Depression and the populations of the Baunt lake valley can still be suggested.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. King, M., Chromosomal Speciation Revisited (Again): Species Evolution. The Role of Chromosome Change, Cambridge Univ. Press, 1993.

    Google Scholar 

  2. Solano, E., Taylor, P.J., Rautenbach, A., et al., Cryptic speciation and chromosomal repatterning in the south african climbing mice Dendromus (Rodentia, Nesomyidae), PLoS One, 2014, vol. 9, no. 2. e88799. https://doi.org/10.1371/journal.pone.0088799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dobigny, G., Britton-Davidian, J., and Robinson, T.J., Chromosomal polymorphism in mammals: an evolutionary perspective, Biol. Rev., 2017, vol. 92, pp. 1—21. https://doi.org/10.1111/brv.12213

    Article  PubMed  Google Scholar 

  4. Silva, W.O.D., Pieczarka, J.C., Ferguson-Smith, M.A., et al., Chromosomal diversity and molecular divergence among three undescribed species of Neacomys (Rodentia, Sigmodontinae) separated by Amazonian rivers, PLoS One, 2017, vol. 12, no. 8. https://doi.org/10.1371/journal.pone.0182218

  5. Romanenko, S.A., Perelman, P.L., Trifonov, V.A., and Graphodatsky, A.S., Chromosomal evolution in Rodentia, Heredity (Edinburg), 2012, vol. 108, no. 1, pp. 4—16. https://doi.org/10.1038/hdy.2011.110

    Article  CAS  PubMed  Google Scholar 

  6. Bannikova, A.A., Lebedev, V.S., Lissovsky, A.A., et al., Molecular phylogeny and evolution of the Asian lineage of vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial cytochrome b sequence, Biol. J. Linn. Soc., 2010, vol. 99, pp. 595—613.

    Article  Google Scholar 

  7. Chaline, J. and Graf, J.D., Phylogeny of the Arvicolidae (Rodentia): biochemical and paleontological evidence, J. Mammal., 1988, vol. 69, no. 1, pp. 22—33.https://doi.org/10.2307/1381744

  8. Zakrzewski, R.J., The fossil record, in Biology of New World Microtus, Tamarin, R.H., Ed., Utah: American Society of Mammalogists, 1985, vol. 8, pp.1—51.

    Google Scholar 

  9. Conroy, C.J. and Cook, J.A., MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents, J. Mammal. Evol., 1999, vol. 6, pp. 221—245.

    Article  Google Scholar 

  10. Musser, G.G. and Carleton, M.D., Order Rodentia, in Mammal Species of the World: A Taxonomic and Geographic Reference, Wilson, D.E. and Reeder, D.M., Eds., Baltimore: Johns Hopkins Univ. Press, 2005, pp. 989—1019.

    Google Scholar 

  11. Malygin, V.M., Sistematika obyknovennoi polevki (Taxonomy of the Common Vole), Moscow: Nauka, 1983.

  12. Modi, W.S., Phylogenetic analyses of chromosomal banding patterns among the Nearctic Arvicolidae (Mammalia, Rodentia), Syst. Zool., 1987, vol. 36, no. 2, pp. 109—136.

    Article  Google Scholar 

  13. Zagorodnyuk, I.V., Karyotypic variation and systematics of gray voles (Rodentia, Arvicolini): 1. Species composition and chromosome numbers, Vestn. Zool., 1990, no. 2, pp. 26—37.

  14. Lemskaya, N.A., Kartavtseva, I.V., Rubtsova, N.V., et al., Chromosome polymorphism in Microtus (Alexandromys) mujanensis (Arvicolinae; Rodentia), Cytogenet. Genome Res., 2015, vol. 146, no. 3, pp. 238—242. https://doi.org/10.1159/000439096

    Article  PubMed  Google Scholar 

  15. Romanenko, S.A., Serdyukova, N.A., Perelman, P.L., et al., Multiple intrasyntenic rearrangements and rapid speciation in voles, Sci. Rep., 2018, vol. 8, no. 1. 14980. https://doi.org/10.1038/s41598-018-33300-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Golenishchev, F.N. and Sablina, O.L., Systematics of the Afghan vole, Microtus (Blanfordimys) afghanus, Zool. Zh., 1991, vol. 70, no. 7, pp. 98—110.

    Google Scholar 

  17. Gromov, I.M. and Polyakov, I.Ya., Fauna SSSR: Mlekopitayushchie (Fauna of the Soviet Union: Mammals), vol. 3, issue 8: Polevki (Microtinae) (Voles (Microtinae)), Leningrad: Nauka, 1977.

  18. Kryštufek, B., Zorenko, T., and Buzan, E.V., New insights into the taxonomy and phylogeny of social voles inferred from mitochondrial cytochrome b sequences, Mamm. Biol., 2012, vol. 77, pp. 178—182. https://doi.org/10.1016/j.mambio.2011.11.007

    Article  Google Scholar 

  19. Golenishchev, F.N. and Malikov, V.G., The “developmental conduit” of the tribe Microtini (Rodentia, Arvicolinae): systematic and evolutionary aspects, Russ. J. Theriol., 2006, vol. 5, no. 1, pp. 19—26.

    Article  Google Scholar 

  20. Lissovsky, A.A., Petrova, T.V., Yatsentyuk, S.P., et al., Multilocus phylogeny and taxonomy of East Asian voles Alexandromys (Rodentia, Arvicolinae), Zool. Scripta, 2018, vol. 47, no. 1, pp. 9—20. https://doi.org/10.1111/zsc.12261

    Article  Google Scholar 

  21. Gileva, E.A., Chromosomal polymorphism in two close forms of subarctic voles (North Siberian vole and Middendorf vole), Dokl. Akad. Nauk SSSR, 1972, vol. 203, no. 2, pp. 689—692.

    CAS  PubMed  Google Scholar 

  22. Orlov, V.N. and Koval’skaya, Yu.M., Microtus mujanensis sp. n. (Rodentia, Cricetidae) from the Vitim River basin, Zool. Zh., 1978, vol. 57, no. 8, pp. 1224—1232.

    Google Scholar 

  23. Gileva, E.A. and Rakitin, S.B., Factors of maintaining chromosome polymorphism in common vole Microtus arvalis Pallas, 1779: reduced fertility and meiotic drive, Russ. J. Genet., 2006, vol. 42, no. 5, pp. 496—504. https://doi.org/10.1134/S1022795406050061

    Article  CAS  Google Scholar 

  24. Baskevich, M.I., Mironova, T.A., Cherepanova, E.V., and Krivonogov, D.M., New data on chromosomal variability, distribution of sibling-species and hybridization of 46-chromosomal forms of Microtus arvalis sensu lato (Rodentia, Arvicolinae) in the Upper Volga river basin, Zool. Zh., 2016, vol. 95, no. 9, pp. 1096—1107.

    Google Scholar 

  25. Sheremetyeva, I.N., Kartavtseva, I.V., and Frisman, L.V., Karyological and allozyme variability of Far Eastern voles Microtus fortis Büchner, 1889 (Cricetidae, Rodentia) from the Russian Far East, Russ. J. Genet., 2006, vol. 42, no. 6, pp. 833—844.

    Article  CAS  Google Scholar 

  26. Meier, M.N., Golenishchev, F.N., Radzhabli, S.I., and Sablina, O.L., Serye polevki fauny Rossii i sopredel’nykh territorii (Voles (Subgenus Microtus Schrank) of Russia and Adjacent Territories), St. Petersburg: Zool. Inst. Russ. Akad. Nauk, 1996.

  27. Wang, J.X., Zhao, X.F., Deng, Y., et al., Chromosomal polymorphism of mandarin vole, Microtus mandarinus (Rodentia), Hereditas, 2003, vol. 133, pp. 47—53.

    Article  Google Scholar 

  28. Baskevich, M.I., Khlyap, L.A., Mironova, T.A., et al., To the problem on stability and variability of the root vole (Microtus oeconomus, Rodentia, Arvicolinae), karyotype: an analysis of new records from Eastern Europe, Zool. Zh., 2016, vol. 95, no. 4, pp. 476—483.

    Google Scholar 

  29. Lamelas, L., Arroyo, M., Fernández, J.F., et al., Structural and evolutionary relationships in the giant sex chromosomes of three Microtus species, Genes, 2018, vol. 9, no. 27. https://doi.org/10.3390/genes9010027

  30. Orlov, V.N. and Koval’skaya, Yu.M., New species of gray voles Microtus mujanensis (Rodentia, Cricetidae) from the Vitim river basin (Transbaikalia), in Sistematika i tsitogenetika mlekopitayushchikh (Systematics and Cytogenetics of Mammals), Moscow: Nauka, 1975, p. 32.

  31. Golenishchev, F.N. and Radzhabli, S.I., A new species of gray vole from the shores of Lake Evoron, Dokl. Akad. Nauk SSSR, 1981, vol. 257, no. 1, pp. 248—250.

    Google Scholar 

  32. Haring, E., Sheremetyeva, I., and Kryukov, A., Phylogeny of Palearctic vole species (genus Microtus, Rodentia) based on mitochondrial sequences, Mammal. Biol., 2011, vol. 76, pp. 258−267.

    Article  Google Scholar 

  33. Voyta, L.L., Golenischev, F.N., and Tiunov, M.P., Analysis of shape and size variation of the first lower molar in Far Eastern grey voles of genus Alexandromys (Rodentia: Cricetidae) from Russian fauna using geometric morphometrics, Russ. J. Theriol., 2013, vol. 12, no. 1, pp. 19—60.

    Article  Google Scholar 

  34. Sheremetyeva, I.N., Kartavtseva, I.V., Vasil’eva, T.V., and Frisman, L.V., Gray voles of the genus Alexandromys from the Verkhnebureinskaya depression, Zool. Zh., 2016, vol. 95, no. 5, pp. 597—603.

    Google Scholar 

  35. Sheremetyeva, I.N., Kartavtseva, I.V., and Vasil’eva, T.V., Does the Evoron vole (Alexandromys evoronensis) inhabit the northeast of the Upper-Zea Plain?, Zool. Zh., 2017, vol. 96, no. 4, pp. 477—474.

    Google Scholar 

  36. Dokuchaev, N.E. and Sheremet’eva, I.N., On the identity of the gray voles (Cricetidae, Rodentia) of the Big Shantar Island (the Sea of Okhotsk) and the Gromov vole (Alexandromys gromovi Vorontsov et al. 1988), Zool. Zh., 2017, vol. 96, no. 11, pp. 1425—1430.

    Google Scholar 

  37. Golenishchev, F.N., Voita, L.L., Abramson, N.I., et al., A new finding of gray voles of the genus Alexandromys in Transbaikalia, Struktura vida u mlekopitayushchikh (Mammalian Species Structure) (Proc. Conf.), Moscow: KMK, 2015.

  38. Sablina, O.V., Radjabli, S.I., and Graphodatsky, A.S., Selected karyotypes, in Atlas of Mammalian Karyotypes, O’Brien, S.J., Nash, W.G., and Menninger, J.C., Eds., 2006, pp. 266—267.

    Google Scholar 

  39. Golenishchev, F.N., Voita, L.L., Moroldoev, I.V., et al., New transbaikalian finds of the muja valley vole (Rodentia: Cricetidae: Alexandromys mujanensis), Tr. Zool. Inst. Ross. Akad. Nauk, 2018, vol. 322, no. 3, pp. 357—384.

    Google Scholar 

  40. Ford, C.F. and Hamerton, J.L., A colchicine hypotonic citrate squash preparation for mammalian chromosomes, Stain Technol., 1956, vol. 31, pp. 247—251.

    Article  CAS  PubMed  Google Scholar 

  41. Grafodatskii, A.S. and Radzhabli, S.I., Khromosomy sel’skokhozyaistvennykh i laboratornykh mlekopitayushchikh. Atlas (Chromosomes of Farm and Laboratory Animals. Atlas), Novosibirsk: Nauka, 1988.

  42. Sitnikova, N.A., Romanenko, S.A., O’Brien, P.C., et al., Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia): 1. The genome homology of tundra vole, field vole, mouse and golden hamster revealed by comparative chromosome painting, Chromosome Res., 2007, vol. 15, pp. 447—456.

    Article  CAS  PubMed  Google Scholar 

  43. Seabright, M., A rapid banding technique for human chromosomes, Lancet, 1971, vol. 2, pp. 971—972.

    Article  CAS  PubMed  Google Scholar 

  44. Yang, F., O’Brien, P.C., Milne, B.S., et al., A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps, Genomics, 1999, vol. 62, pp. 189—202.

    Article  CAS  PubMed  Google Scholar 

  45. Graphodatsky, A.S., Yang, F., O’Brien, P.C., et al., A comparative chromosome map of the Arctic fox, red fox and dog defined by chromosome painting and high resolution G-banding, Chromosome Res., 2000, vol. 8, no. 3, pp. 253—263.

    Article  CAS  PubMed  Google Scholar 

  46. 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  CAS  PubMed  PubMed Central  Google Scholar 

  47. Sheremet’eva, I.N., Kartavtseva, I.V., Pavlenko, M.V., et al., Genetic variability of the peripheral population of the greater long-tailed hamster Tscherskia triton (De Winton 1899) in the northeastern part of the distribution range based on sequencing data of the control region of mitochondrial DNA, Biol. Bull., 2017, vol. 44, no. 4, pp. 391—400. https://doi.org/10.1134/S1062359017040136

  48. Sheremetyeva, I.N., Kartavtseva, I.V., Frisman, L.V., et al., Polymorphism and genetic structure of Microtus maximowiczii (Schrenck, 1858) (Rodentia, Cricetidae) from the Middle Amur River region as inferred from sequencing of the mtDNA control region, Russ. J. Genet., 2015, vol. 51, no. 10, pp. 992—999. https://doi.org/10.1134/S1022795415100166

    Article  CAS  Google Scholar 

  49. Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Symp., 1999, no. 41, pp. 95—98.

  50. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, no. 12, pp. 2725—2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  52. Tajima, F., Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism, Genetics, 1989, no. 123, pp. 585—595.

  53. Fu, Y.X., Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection, Genetics, 1997, no. 147, pp. 915—925.

  54. 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.

    Article  CAS  Google Scholar 

  55. Hudson, R.R., Boos, D.D., and Kaplan, N.L., A statistical test for detecting population subdivision, Mol. Biol. Evol., 1992, no. 9, pp. 138—151.

  56. Kartavtseva, I.V. and Kryukov, A.P., Karyotype of Microtus fortis (Rodentia, Cricetidae) from extreme south of Far East Russia, Chromosome Sci., 1998, vol. 2, pp. 31—34.

    Google Scholar 

  57. Avise J.C. Phylogeography: The History and Formation of Species, Cambridge, MA: Harvard Univ. Press, 2000.

    Google Scholar 

  58. Enikeev, F.I. and Staryshko, V.E., Glyatsial’nyi morfogenez i rossypeobrazovanie Vostochnogo Zabaikal’ya (Glacial Morphogenesis of Placers in East Transbaikalia), Chita: Chita Gos. Univ., 2009.

  59. Enikeev, F.I. and Staryshko, V.E., Glaciers of the Kodar Range (Northern Transbaikalia), Geogr. Prir. Res., 2014, no. 1, pp. 107—117.

Download references

Funding

This study was supported by the state contract with the Laboratory of Evolutionary Zoology and Genetics, Federal Center for Terrestrial Biota Diversity of East Asia, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, no. AAAA-А17-117062710083-0 and the Laboratory of Theriology, Zoological Institute, Russian Academy of Sciences, St. Petersburg, no. AAAA-A17-117022810195-3, and the Russian Foundation for Basic Research (grant nos. 12-04-00662a, 14-04-31555, 15-04-03871, and 19-04-00557a).

Author information

Authors and Affiliations

  1. Federal Center for Terrestrial Biota Diversity of East Asia, Far Eastern Branch, Russian Academy of Sciences, 690022, Vladivostok, Russia

    I. V. Kartavtseva, T. V. Vasilieva & I. N. Sheremetyeva

  2. Institute of Molecular and Cellular Biology, Siberian Branch, Russian Academy of Sciences, 630090, Novosibirsk, Russia

    N. A. Lemskaya

  3. Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, 630091, Novosibirsk, Russia

    I. V. Moroldoev

  4. Zoological Institute, Russian Academy of Sciences, 199034, St. Petersburg, Russia

    F. N. Golenishchev

Authors
  1. I. V. Kartavtseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. V. Vasilieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. N. Sheremetyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. A. Lemskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I. V. Moroldoev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. N. Golenishchev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to I. V. Kartavtseva or I. N. Sheremetyeva.

Ethics declarations

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

CONFLICT OF INTEREST

The authors declare that they have no conflicts of interest.

Additional information

Translated by N. Maleeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kartavtseva, I.V., Vasilieva, T.V., Sheremetyeva, I.N. et al. Genetic Variability of Three Isolated Populations of the Muya Valley Vole Alexandromys mujanensis Orlov et Kovalskaja, 1978 (Rodentia, Arvicolinae). Russ J Genet 55, 978–992 (2019). https://doi.org/10.1134/S1022795419080076

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795419080076

Keywords:

Search

Navigation