Abstract
The four species of common voles within the genus Microtus – M. 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.
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.
Catze£is FM, Aguilar J-P, Jaeger J-J (1992) Muroid rodents: phylogeny and evolution. Tree 7: 12–126.
Elder FF (1980) Tandem fusion, centric fusion, and chromosomal evolution in the cotton rats, genus Sigmodon. Cytogenet Cell Genet 26: 19–210.
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.
Felsenstein J (1985) Con¢dence limits on phylogenesis: an approach using the bootstrap. Evolution 39: 78–791.
Felsenstein J (1993) PHYLIP (Phylogenetic Inference Package), version 3.5C, Dept. of Genetics, Univ. of Washington, Seattle.
Gissi C, Reyes A, Pesole G, Saccone C (2000) Lineage-speci¢c evolutionary rate in mammalian mtDNA. Mol Biol Evol 17: 102–31.
Graphodatsky AS (1981) Nucleolus organiser regions of the chromosomes of domestic pig. Tsitologiya i Genetica 15: 2–31.
Graphodatsky AS, Radjabli SI (1988) Chromosomes of farm and laboratory mammals. Novosibirsk: Nauka.
Gromov IM, Polyakov IY (1977) The fauna of Russia. Mammals. Voles (Microtinae). Leningrad: Nauka.
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.
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.
Kimura M. (1980) A simplemethod for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16: 11–120.
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.
Kuhner MK, Felsenstein J (1994) A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol Biol Evol 11: 45–68.
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.
Malygin VM (1983) Systematics of common voles. Moscow: Nauka.
Malygin VM, Sablina OV (1994) Karyotypes. In: Sokolov VE & Bashenina NV, eds. Common vole: the sibling species. Moscow: Nauka, pp.7-25.
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.
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.
Mazurok NA, Nesterova TB, Zakian SM (1995) High-resolution G-banding of chromosomes in Microtus subarvalis (Rodentia, Arvicolidae). Hereditas 123: 4–52.
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.
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.
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.
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.
Meyer MN, Orlov VN, Sholl ED (1972) Sibling species in Microtus arvalis group (Rodentia, Cricetidae). Zool J 51: 724–738.
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.
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.
Modi WS (1987) Phylogenetic analyses of chromosomal band-ing patterns among the nearctic Arvicolidae (Mammalia, Rodentia). Syst Zool 36: 10–136.
Murray V (1989) Improved double-stranded DNA sequencing using linear polymerase chain reaction. Nucl Acid Res 17: 8–89.
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.
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.
Nesterova TB, Mazurok NA, Rubtsova NV, Isaenko AA, Zakian SM (1998b) The vole gene map. ILAR J 39: 13–144.
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.
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.
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.
Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2: 97–972.
Shevchenko AI, Slobodyanyuk SY, Zakiyan SM (1999) Varia-bility of DNA repeats in four species of common voles. Moleculyarnaya Biologia 33: 62–627.
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.
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.
Yoder AD, Yang Z (2000) Estimation of primate speciation dates using local molecular clocks. Mol Biol Evol 17: 108–90.
Zagorodnyuk IV (1991) Karyotypic variability of 46–chromosome forms of Microtus arvalis (Rodentia) voles: taxinomic estimate. Vestnik Zoologii 1: 3–45.
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.
Rights 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
Issue Date:
DOI: https://doi.org/10.1023/A:1009226918924