Chromosome Research

, Volume 24, Issue 2, pp 145–159 | Cite as

Genome-wide comparative chromosome maps of Arvicola amphibius, Dicrostonyx torquatus, and Myodes rutilus

  • Svetlana A. RomanenkoEmail author
  • Natalya A. Lemskaya
  • Vladimir A. Trifonov
  • Natalya A. Serdyukova
  • Patricia C.M. O’Brien
  • Nina Sh. Bulatova
  • Feodor N. Golenishchev
  • Malcolm A. Ferguson-Smith
  • Fengtang Yang
  • Alexander S. Graphodatsky


The subfamily Arvicolinae consists of a great number of species with highly diversified karyotypes. In spite of the wide use of arvicolines in biological and medicine studies, the data on their karyotype structures are limited. Here, we made a set of painting probes from flow-sorted chromosomes of a male Palearctic collared lemming (Dicrostonyx torquatus, DTO). Together with the sets of painting probes made previously from the field vole (Microtus agrestis, MAG) and golden hamster (Mesocricetus auratus, MAU), we carried out a reciprocal chromosome painting between these three species. The three sets of probes were further hybridized onto the chromosomes of the Eurasian water vole (Arvicola amphibius) and northern red-backed vole (Myodes rutilus). We defined the diploid chromosome number in D. torquatus karyotype as 2n = 45 + Bs and showed that the system of sex chromosomes is X1X2Y1. The probes developed here provide a genomic tool-kit, which will help to investigate the evolutionary biology of the Arvicolinae rodents. Our results show that the syntenic association MAG1/17 is present not only in Arvicolinae but also in some species of Cricetinae; and thus, should not be considered as a cytogenetic signature for Arvicolinae. Although cytogenetic signature markers for the genera have not yet been found, our data provides insight into the likely ancestral karyotype of Arvicolinae. We conclude that the karyotypes of modern voles could have evolved from a common ancestral arvicoline karyotype (AAK) with 2n = 56 mainly by centric fusions and fissions.


Comparative cytogenetics Karyotype evolution Voles Lemming 



Arvicola amphibius


Alexandromys oeconomus (here and further in the text, the species nomenclature is used in accordance with the latest checklist “The mammals of Russia: a taxonomic and geographic reference” (Pavlinov and Lissovsky 2012))


Myodes rutilus




Dicrostonyx torquatus


Evolutionary new centromeres


Fluorescence in situ hybridization


G-banding by trypsin using Giemsa




Interstitial telomeric sequences


Microtus agrestis


Mesocricetus auratus





This study was funded in part by the MCB and SB RAS Programs, research grants of Russian Fund for Basic Research (No. 11-04-00673, No. 14-04-00451 (SAR); No. 14-04-31555 (NAL); No. 15-29-02384, No. 15-04-00962 (ASG)) and ZIN RAS (project No. 01201351185).

Compliance with ethical standards

All institutional and national guidelines for the care and use of laboratory animals were followed.

Conflict of interest

The authors declare that they have no competing of interests.

Supplementary material

10577_2015_9504_MOESM1_ESM.doc (74 kb)
ESM 1 (DOC 74 kb)
10577_2015_9504_MOESM2_ESM.pdf (286 kb)
ESM 2 (PDF 286 kb)
10577_2015_9504_MOESM3_ESM.xls (35 kb)
ESM 3 (XLS 35 kb)


  1. Abramson NI, Lebedev VS, Bannikova AA, Tesakov AS (2009a) Radiation events in the subfamily Arvicolinae (Rodentia): evidence from nuclear genes. Dokl Biol Sci 428:458–461CrossRefPubMedGoogle Scholar
  2. Abramson NI, Lebedev VS, Tesakov AS, Bannikova AA (2009b) Supraspecies relationships in the subfamily (Rodentia, Cricetidae, Arvicolinae): unexpexted result of nuclear genes analysis. Mol Biol (Mosk) 43:897–909CrossRefGoogle Scholar
  3. Abramson NI, Golenishchev FN, Kostygov AYu, Tesakov AS (2011) Taxonomic interpretation of molecular-genetic cladogram for voles of the tribe Mocrotini (Arvicolinae, Rodentia) inferred from nuclear genes. In: Theriofauna of Russia and adjacement regions, 9th Congress of Theriological Society. KMK Sci. Press, Moscow, p. 7Google Scholar
  4. Acosta MJ, Marchal JA, Fernandez-Espartero C et al (2010) Characterization of the satellite DNA Msat-160 from species of Terricola (Microtus) and Arvicola (Rodentia, Arvicolinae). Genetica 138:1085–1098CrossRefPubMedGoogle Scholar
  5. Bakloushinskaya IY, Matveevsky SN, Romanenko SA et al (2012) A comparative analysis of the mole vole sibling species Ellobius tancrei and E. talpinus (Cricetidae, Rodentia) through chromosome painting and examination of synaptonemal complex structures in hybrids. Cytogenet Genome Res 136:199–207CrossRefPubMedGoogle Scholar
  6. Bannikova AA, Lebedev VS, Lissovsky AA et al (2010) Molecular phylogeny and evolution of the Asian lineage of vole genus Microtus (Rodentia: Arvicolinae) inferred from mitochondrial cytochrome b sequence. Biol J Linn Soc 99:595–613CrossRefGoogle Scholar
  7. Borodin PM, Sablina OV, Rodionova MI (1995) Pattern of X-Y chromosome pairing in microtine rodents. Hereditas 123:17–23CrossRefPubMedGoogle Scholar
  8. Carleton MD, Musser GG (2005) Subfamily Arvicolinae. In: Wilson E, Reeder D-AM (eds) Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore, pp. 956--1039Google Scholar
  9. Chaline J, Graf JD (1988) Phylogeny of the Arvicolidae (Rodentia)—biochemical and paleontological evidence. J Mammal 69:22–33CrossRefGoogle Scholar
  10. Chernyavsky FB, Kozlovsky AI (1980) Species status and history of the Arctic lemming (Dicrostonyx, Rodentia) of Wrangel Island. Zool Zh (in Russian) 59:266–273Google Scholar
  11. Conroy C, Cook JA (1999) MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. J Mamm Evol 6:221–245CrossRefGoogle Scholar
  12. Cook JA, Runck AM, Conroy CJ (2004) Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Mol Phylogenet Evol 30:767–777CrossRefPubMedGoogle Scholar
  13. de la Fuente R, Sanchez A, Marchal JA et al (2012) A synaptonemal complex-derived mechanism for meiotic segregation precedes the evolutionary loss of homology between sex chromosomes in arvicolid mammals. Chromosoma 121:433–446CrossRefPubMedGoogle Scholar
  14. DeWoody JA, Chesser RK, Baker RJ (1999) A translocated mitochondrial cytochrome b pseudogene in voles (Rodentia: Microtus). J Mol Evol 48:380–382CrossRefPubMedGoogle Scholar
  15. Fredga K (1983) Aberrant sex chromosome mechanisms in mammals. Evol asp Differ 23(Suppl):S23–30Google Scholar
  16. Fredga K, Fedorov V, Jarrell G, Jonsson L (1999) Genetic diversity in Arctic lemmings. Ambio 28:261--269Google Scholar
  17. Galewski T, Tilak MK, Sanchez S et al (2006) The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evol Biol 6:80CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gileva EA (1980) Chromosomal diversity and an aberrant genetic system of sex determination in the arctic lemming, Dicrostonyx-torquatus pallas (1779). Genetica 52–3:99–103Google Scholar
  19. Gileva EA (1983) A contrasted pattern of chromosome evolution in 2 genera of lemmings, Lemmus and Dicrostonyx (Mammalia, Rodentia). Genetica 60:173–179CrossRefGoogle Scholar
  20. Gileva EA (2004) The B chromosome system in the varying lemming Dicrostonyx torquatus pall., 1779 from natural and laboratory populations. Russ J Genet 40:1399–1406CrossRefGoogle Scholar
  21. Gileva EA, Chebotar NA (1979) Fertile XO males and females in the varying lemming, Dicrostonyx torquatus pall. 1779. Heredity 42:67–77CrossRefGoogle Scholar
  22. Graphodatsky AS, Sablina OV, Meyer MN et al (2000) Comparative cytogenetics of hamsters of the genus Calomyscus. Cytogenet Cell Genet 88:296–304CrossRefPubMedGoogle Scholar
  23. Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG) n generated by PCR. Nucleic Acids Res 19:4780CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jaarola M, Martinkova N, Gunduz I et al (2004) Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 33:647–663CrossRefPubMedGoogle Scholar
  25. Lemskaya NA, Romanenko SA, Golenishchev FN et al (2010) Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). III. Karyotype relationships of ten Microtus species. Chromosome Res 18:459–471CrossRefPubMedGoogle Scholar
  26. Li T, Wang J, Su W, Nie W, Yang F (2006) Karyotypic evolution of the family Sciuridae: inferences from the genome organizations of ground squirrels. Cytogenet Genome Res 112:270–276CrossRefPubMedGoogle Scholar
  27. Maden BE, Dent CL, Farrell TE et al (1987) Clones of human ribosomal DNA containing the complete 18 S-rRNA and 28 S-rRNA genes. Characterization, a detailed map of the human ribosomal transcription unit and diversity among clones. Biochem J 246:519–527CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mazurok NA, Rubtsova NV, Isaenko AA et al (2001) Comparative chromosome and mitochondrial DNA analyses and phylogenetic relationships within common voles (Microtus, Arvicolidae). Chromosome Res 9:107–120CrossRefPubMedGoogle Scholar
  29. Modi WS (1987a) C-banding analyses and the evolution of heterochromatin among arvicolid rodents. J Mammal 68:704–714CrossRefGoogle Scholar
  30. Modi WS (1987b) Phylogenetic analyses of chromosomal banding-patterns among the Nearctic Arvicolidae (Mammalia, Rodentia). Syst Zool 36:109–136CrossRefGoogle Scholar
  31. Orlov VN, Bulatova NSh (1983) Comparative cytogenetics and karyosystematic of mammals. Nauka, Moscow (In russian)Google Scholar
  32. Pavlinov IYa, Lissovsky AA (2012) The mammals of Russia: a taxonomic and geographic reference. In: Kalyakin MV (ed) Archives of zoological museum of Moscow state university. KMK Scientific Press Ltd, Moscow, pp. 1--604Google Scholar
  33. Repenning CA (1990) Of mice and ice in the Late Pliocene of North-America. Arctic 43:314--323Google Scholar
  34. Romanenko SA, Volobouev V (2012) Non-sciuromorph rodent karyotypes in evolution. Cytogenet Genome Res 137:233–245CrossRefPubMedGoogle Scholar
  35. Romanenko SA, Perelman PL, Serdukova NA et al (2006) Reciprocal chromosome painting between three laboratory rodent species. Mamm Genome 17:1183–1192CrossRefPubMedGoogle Scholar
  36. Romanenko SA, Sitnikova NA, Serdukova NA et al (2007) Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). II. The genome homology of two mole voles (genus Ellobius), the field vole and golden hamster revealed by comparative chromosome painting. Chromosome Res 15:891–897CrossRefPubMedGoogle Scholar
  37. Romanenko SA, Perelman PL, Trifonov VA, Graphodatsky AS (2012) Chromosomal evolution in Rodentia. Heredity (Edinb) 108:4–16CrossRefGoogle Scholar
  38. Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 11:971–972CrossRefGoogle Scholar
  39. Sitnikova NA, Romanenko SA, O'Brien PC et al (2007) Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). I. The genome homology of tundra vole, field vole, mouse and golden hamster revealed by comparative chromosome painting. Chromosome Res 15:447–456CrossRefPubMedGoogle Scholar
  40. Telenius H, Pelmear AH, Tunnacliffe A et al (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosom Cancer 4:257–263CrossRefPubMedGoogle Scholar
  41. Triant DA, Dewoody JA (2006) Accelerated molecular evolution in Microtus (Rodentia) as assessed via complete mitochondrial genome sequences. Genetica 128:95–108CrossRefPubMedGoogle Scholar
  42. Trifonov VA, Kosyakova N, Romanenko SA et al (2010) New insights into the karyotypic evolution in muroid rodents revealed by multicolor banding applying murine probes. Chromosom Res 18:265–275CrossRefGoogle Scholar
  43. Weimer J, Kiechle M, Arnold N (2000) FISH-microdissection (FISH-MD) analysis of complex chromosome rearrangements. Cytogenet Cell Genet 88:114–118CrossRefPubMedGoogle Scholar
  44. Yang F, Carter NP, Shi L, Ferguson-Smith MA (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103:642–652CrossRefPubMedGoogle Scholar
  45. Yang F, O'Brien PC, Milne BS et al (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62:189–202CrossRefPubMedGoogle Scholar
  46. Yannic G, Burri R, Malikov VG, Vogel P (2012) Systematics of snow voles (Chionomys, Arvicolinae) revisited. Mol Phylogenet Evol 62:806–815CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Svetlana A. Romanenko
    • 1
    • 2
    Email author
  • Natalya A. Lemskaya
    • 1
  • Vladimir A. Trifonov
    • 1
    • 2
  • Natalya A. Serdyukova
    • 1
  • Patricia C.M. O’Brien
    • 3
  • Nina Sh. Bulatova
    • 4
  • Feodor N. Golenishchev
    • 5
  • Malcolm A. Ferguson-Smith
    • 3
  • Fengtang Yang
    • 6
  • Alexander S. Graphodatsky
    • 1
  1. 1.Institute of Molecular and Cellular BiologyNovosibirskRussia
  2. 2.Novosibirsk State UniversityNovosibirskRussia
  3. 3.Department of Veterinary Medicine, Cambridge Resource Centre for Comparative GenomicsUniversity of CambridgeCambridgeUK
  4. 4.A. N. Severtsov Institute of Ecology and EvolutionMoscowRussia
  5. 5.Zoological Institute, RASSaint-PetersburgRussia
  6. 6.Wellcome Trust Sanger InstituteWellcome Trust Genome CampusCambridgeUK

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