Skip to main content
Log in

Comparative chromosome and mitochondrial DNA analyses and phylogenetic relationships within common voles (Microtus, Arvicolidae)

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

The four species of common voles within the genus MicrotusM. kirgisorum, M. transcaspicus, M. arvalis, and M. rossiaemeridionalis – are so closely related that neither morphological features nor paleontological evidence allow clarification of their phylogeny. Analysis of vole karyotypes and mitochondrial DNA sequences, therefore, is essential for determining their phylogenetic relationships. A comparison of high resolution GTG-banding patterns allows us to ascertain the similarity between the karyotypes of these species, revealing that they are composed of rearrangements of the same chromosomal elements. Based on this analysis, we propose possible routes of chromosomal divergence involved in speciation within this group of voles and construct a phylogenetic tree of their karyotypes. We suggest that two different karyotypic variants existed during the course of vole evolution – one resulting in M. rossiaemeridionalis and M. transcaspicus, the other, M. kirgisorum and M. arvalis. As an alternative approach FITCH and KITSCH computer programs were used to construct a phylogenetic tree of vole molecular evolution based on a pairwise comparison of mitochondrial cytochrome b sequences and the divergence time of the species was determined. The correlation between the trees constructed using karyologic and molecular approaches is discussed in the context of other available data.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bromham L, Penny D, Rambaut A, Hendy MD (2000) The power of relative rates tests depends on the data. JMol Evol 50: 29–301.

    Google Scholar 

  • Catze£is FM, Aguilar J-P, Jaeger J-J (1992) Muroid rodents: phylogeny and evolution. Tree 7: 12–126.

    Google Scholar 

  • Elder FF (1980) Tandem fusion, centric fusion, and chromosomal evolution in the cotton rats, genus Sigmodon. Cytogenet Cell Genet 26: 19–210.

    Google Scholar 

  • Elisaphenko EA, Nesterova TB, Duthie SM et al. (1998) Repetitive DNA sequences in the common vole: cloning, characterisation and chromosome localisation of two novel complex repeats MS3 and MS4 from the genome of the East European vole Microtus rossiaemeridionalis. Chrom Res 6: 35–360.

    Google Scholar 

  • Felsenstein J (1985) Con¢dence limits on phylogenesis: an approach using the bootstrap. Evolution 39: 78–791.

    Google Scholar 

  • Felsenstein J (1993) PHYLIP (Phylogenetic Inference Package), version 3.5C, Dept. of Genetics, Univ. of Washington, Seattle.

    Google Scholar 

  • Gissi C, Reyes A, Pesole G, Saccone C (2000) Lineage-speci¢c evolutionary rate in mammalian mtDNA. Mol Biol Evol 17: 102–31.

    Google Scholar 

  • Graphodatsky AS (1981) Nucleolus organiser regions of the chromosomes of domestic pig. Tsitologiya i Genetica 15: 2–31.

    Google Scholar 

  • Graphodatsky AS, Radjabli SI (1988) Chromosomes of farm and laboratory mammals. Novosibirsk: Nauka.

    Google Scholar 

  • Gromov IM, Polyakov IY (1977) The fauna of Russia. Mammals. Voles (Microtinae). Leningrad: Nauka.

    Google Scholar 

  • Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal devel-oper: a 1–step method. Experientia 36: 101–1015.

    Google Scholar 

  • Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Paabo S (1994) The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137: 24–56.

    Google Scholar 

  • Kimura M. (1980) A simplemethod for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16: 11–120.

    Google Scholar 

  • Kocher TB, Thomas WK, Meyer A et al. (1989) Dynamics of mitochondrial DNA evolution in animals: ampli¢cation and sequencing with conserved primers. Proc Nat. Acad Sci USA 86: 619–6200.

    Google Scholar 

  • Kuhner MK, Felsenstein J (1994) A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol Biol Evol 11: 45–68.

    Google Scholar 

  • Lee C, Sasi R, Lin CC (1993) Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs. Cytogenet Cell Genet 63: 15–9.

    Google Scholar 

  • Malygin VM (1983) Systematics of common voles. Moscow: Nauka.

    Google Scholar 

  • Malygin VM, Sablina OV (1994) Karyotypes. In: Sokolov VE & Bashenina NV, eds. Common vole: the sibling species. Moscow: Nauka, pp.7-25.

    Google Scholar 

  • Matthey R (1973) The chromosome formulae of eutherian mammals. In: Chiarelli AB & Capanna F, eds. Cytotaxonomy and vertebrate evolution. Academic Press: London and New York, pp. 53–616.

    Google Scholar 

  • Mazurok NA, Rubtsov NB, Nesterova TB, Zakian SM (1994) High-resolution G-banding of chromosomes in Microtus kirgisorum (Muridae, Rodentia). Cytogenet Cell Genet 67: 20–210.

    Google Scholar 

  • Mazurok NA, Nesterova TB, Zakian SM (1995) High-resolution G-banding of chromosomes in Microtus subarvalis (Rodentia, Arvicolidae). Hereditas 123: 4–52.

    Google Scholar 

  • Mazurok NA, Isaenko AA, Nesterova TB, Zakian SM (1996a) High-resolution G-banding of chromosomes in the common vole Microtus arvalis (Rodentia, Arvicolidae). Hereditas 124: 22–232.

    Google Scholar 

  • Mazurok NA, Rubtsova NV, Isaenko AA, Nesterova TB, Zakian SM (1996b) Comparative analysis of chromosomes in Microtus transcaspicus and Microtus subarvalis (Arvicolidae, Rodentia): high-resolution G-banding and localisation of NORs. Hereditas 124: 24–250.

    Google Scholar 

  • Meulen AJ (1978) Microtus and Pitymys (Arvicolidae) from Cumberland Cave, Maryland, with a comparison of some new and old world species. Ann Carnegie Mus 47: 10–145.

    Google Scholar 

  • Meyer A, Kocher TB, Basasiwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid ¢shes suggested by mitochondrial DNA sequences. Nature 347: 55–553.

    Google Scholar 

  • Meyer MN, Orlov VN, Sholl ED (1972) Sibling species in Microtus arvalis group (Rodentia, Cricetidae). Zool J 51: 724–738.

    Google Scholar 

  • Meyer MN, Radjabli SI, Bulatova NS, Golenishchev FN(1985) Karyological pecularities and probable relations of common voles of the group ``arvalis'' (Rodentia, Cricetidae, Microtus). Zool J 64: 41–428.

    Google Scholar 

  • Meyer MN, Golenishchev FN, Radjabli SI, Sablina OV (1996) Grey voles (Subgenus Microtus) of the fauna of Russia and adjacent territories. Trans Zool Inst Ross Akad Nauk (St. Petersburg), 232: 9–112.

    Google Scholar 

  • Modi WS (1987) Phylogenetic analyses of chromosomal band-ing patterns among the nearctic Arvicolidae (Mammalia, Rodentia). Syst Zool 36: 10–136.

    Google Scholar 

  • Murray V (1989) Improved double-stranded DNA sequencing using linear polymerase chain reaction. Nucl Acid Res 17: 8–89.

    Google Scholar 

  • Nesterova TB, Mazurok NA, Matveeva NMet al. (1994) Dem-onstration of the X-linkage and order of the genes GLA, G6PD, HPRT and PGK in two vole species of the genus Microtus. Cytogenet Cell Genet 64: 25–255.

    Google Scholar 

  • Nesterova TB, Duthie SM, Mazurok NA et al. (1998a) Com-parative mapping of X chromosomes in rat and ¢ve vole species of the genus Microtus. Chrom Res 6: 4–48.

    Google Scholar 

  • Nesterova TB, Mazurok NA, Rubtsova NV, Isaenko AA, Zakian SM (1998b) The vole gene map. ILAR J 39: 13–144.

    Google Scholar 

  • Orlov VN, Malygin VM (1969) Two forms of 46 chromosome Microtus arvalis Pallas. In: Vorontsov NN, ed. The Mammals (evolution, karyology, systematics, faunistics). Materials of the 2nd All-Union Symposium on Mammals. Novosibirsk: Nauka, pp. 14–144.

    Google Scholar 

  • Rubtsov N, Graphodatsky A, Matveeva VG et al. (1988) Silver fox gene mapping: conserved chromosome regions in the order Carnivora. Cytogenet Cell Genet 48: 9–98.

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Second edition, Vol. I-III, Cold Spring Harbor: New York.

    Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2: 97–972.

    Google Scholar 

  • Shevchenko AI, Slobodyanyuk SY, Zakiyan SM (1999) Varia-bility of DNA repeats in four species of common voles. Moleculyarnaya Biologia 33: 62–627.

    Google Scholar 

  • Wilcox TP, Hugg L, Zeh JA, Zeh DW (1997) Mitochondrial DNA sequencing reveals extreme genetic differentiation in a cryptic species complex of neotropical pseudoscorpions. Mol Phylogenet Evol 7: 20–216.

    Google Scholar 

  • Yang F, O'Brien PCM, Wienberg J, Neitzel H, Lin CC, Fer-guson-Smith MA (1997) Chromosomal evolution of the Chinese muntjac (Muntiacus reevesi). Chromosoma 106: 3–43.

    Google Scholar 

  • Yoder AD, Yang Z (2000) Estimation of primate speciation dates using local molecular clocks. Mol Biol Evol 17: 108–90.

    Google Scholar 

  • Zagorodnyuk IV (1991) Karyotypic variability of 46–chromosome forms of Microtus arvalis (Rodentia) voles: taxinomic estimate. Vestnik Zoologii 1: 3–45.

    Google Scholar 

  • Zakian SM, Nesterova TB, Cheryaukene OV, Bochkarev MN (1991) Heterochromatin as a factor affecting the inactivation of X-chromosome in interspeci¢c hybrid voles (Microtidae, Rodentia). Genet Res 58: 10–110.

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mazurok, N.A., Rubtsova, N.V., Isaenko, A.A. et al. Comparative chromosome and mitochondrial DNA analyses and phylogenetic relationships within common voles (Microtus, Arvicolidae). Chromosome Res 9, 107–120 (2001). https://doi.org/10.1023/A:1009226918924

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1009226918924

Navigation