Jump to ContentJump to Main Navigation
Show Summary Details
More options …


More options …
Volume 69, Issue 1


Intraspecific epigenetic polymorphism of the East European vole (Microtus levis Miller, 1908) in South-eastern Europe and Turkey

Georgi Markov
  • Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Bul. “Tzar Osvobiditel” No. 1, 1000, Sofia, Bulgaria
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Nuri Yiğit / Ercüment Çolak / Maria Kocheva
  • Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Bul. “Tzar Osvobiditel” No. 1, 1000, Sofia, Bulgaria
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Milena Gospodinova
  • Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Bul. “Tzar Osvobiditel” No. 1, 1000, Sofia, Bulgaria
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2013-11-15 | DOI: https://doi.org/10.2478/s11756-013-0288-x


This study aims to represent the first report on population variation of 20 non-metric skull characters in East European vole (Microtus levis) from the Balkan (populations from Northern Dobruja; Southern Dobruja; East part of the Danube Plain; North-east Trace; Sofia field; South-east Trace) and Anatolian peninsulas (populations from North-west Anatolia region and Central Anatolia region), on the basis of which to determine its epigenetic variability and to analyse their mutual geographical epigenetic relations through comparison of the epigenetic divergence among them. Estimation of epigenetic variation of the studied populations of M. levis showed similar pattern of variation, but it is mostly higher than the other rodent species with a similar range of distribution, such as Microtus arvalis, Mus musculus, Apodemus sylvaticus, Apodemus flavicollis and Clethrionomys glareolus. Each one of the studied traits manifested some polymorphism. Moreover, all the calculated epigenetic distances (MMD) were statistically insignificant (P < 0.05) and epigenetic cranial uniqueness (MU) of any studied population was not found. These results reveal lack of expressed geographic relationship of population epigenetic variability in East European vole. The revealed populations epigenetic polymorphism of M. levis gives an opportunity for more complete assessment of variability and biological diversity of this species, but further research is necessary to elucidate its population epigenetics, especially as the data obtained in recent investigations of cranial morphology of the sibling species from the group the M. arvalis (sensu lato) added new locations to the distribution map of the East European vole in Eurasia.

Keywords: non-metric characters; epigenetic variation; population epigenetic; Microtus levis

  • [1] Ansorge H. 2001. Assessing non-metric skeleton characters as a morphological tool. Zoology 104(3–4): 268–277. DOI: 10.1078/0944-2006-00032 http://dx.doi.org/10.1078/0944-2006-00032CrossrefGoogle Scholar

  • [2] Ansorge H., Anděra M., Borkenhagen P., Büchner S., Juškaitis R. & Markov G. 2012. Morphological approach to the genetic variability of the common dormouse Muscardinus avellanarius. Peckiana 8: 265–274. Google Scholar

  • [3] Bashenina N.V. 1953. K voprosu ob opredelenii vozrasta obyknovennoi polevki (Microtus arvalis Pall.) [On age determination of common vole (Microtus arvalis Pall.)]. Zool. Zh. 32(4): 730–743 Google Scholar

  • [4] Bauchau V. 1988. Non-metrical variation in wild mammals: a bibliography. Mammal Rev. 18(4): 195–200. DOI: 10.1111/j.1365-2907.1988.tb00085.x http://dx.doi.org/10.1111/j.1365-2907.1988.tb00085.xCrossrefGoogle Scholar

  • [5] Berry R.J. 1963. Epigenetic polymorphism in wild populations of Mus musculus. Gen. Res. Camb. 4(2): 193–220. DOI: http://dx.doi.org/10.1017/S0016672300003566 http://dx.doi.org/10.1017/S0016672300003566CrossrefGoogle Scholar

  • [6] Berry R.J. 1975. On the nature of genetical distance and island races of Apodemus sylvaticus. J. Zool. 176(2): 292–295. DOI: 10.1111/j.1469-7998.1975.tb03201.x http://dx.doi.org/10.1111/j.1469-7998.1975.tb03201.xCrossrefGoogle Scholar

  • [7] Berry R.J. & Jakobson M.E. 1975. Ecological genetics of an island population of the house mouse (Mus musculus). J. Zool. Lond. 175(4): 523–540. DOI: 10.1111/j.1469-7998.1975.tb01415.x http://dx.doi.org/10.1111/j.1469-7998.1975.tb01415.xCrossrefGoogle Scholar

  • [8] Berry R.J., Jakobson M.E. & Peters J. 1978. The house mice of the Faroe Islands: a study in micro differentiation. J. Zool. Lond. 185: 73–92. http://dx.doi.org/10.1111/j.1469-7998.1978.tb03314.xCrossrefGoogle Scholar

  • [9] Berry R.J. & Searle A.G. 1963. Epigenetic polymorphism in rodents. Proc. Zool. Soc. Lond. 140(4): 577–615. DOI: 10.1111/j.1469-7998.1963.tb01990.x CrossrefGoogle Scholar

  • [10] Burkey T.V. 1995. Extinction rates in archipelagos: implications for populations in fragmented habitats. Cons. Biol. 9(3): 527–541. DOI: 10.1046/j.1523-1739.1995.09030527.x http://dx.doi.org/10.1046/j.1523-1739.1995.09030527.xCrossrefGoogle Scholar

  • [11] Hedges S.R. 1969. Epigenetic polymorphism in populations of Apodemus sylvaticus and Apodemus flavicollis (Rodentia, Muridae). J. Zool. 159(4): 425–442. DOI: 10.1111/j.1469-7998.1969.tb03899.x http://dx.doi.org/10.1111/j.1469-7998.1969.tb03899.xCrossrefGoogle Scholar

  • [12] Kalcheva V. & Topashka-Ancheva M. 2005. New data on the karyotype heterogeneity of Microtus rossiaemeridionalis (Ognev, 1924) from Northeastern Bulgaria. Comptes rendus de l’Académie bulgare des Science [Proceeding of the Bulgarian Academy of Sciences] 58(7): 827–832. Google Scholar

  • [13] Lazarová J. 1999. Epigenetic variation and fluctuating asymmetry of the house mouse (Mus) in the Czech Republic. Folia Zool. 48(Suppl. 1): 37–52. Google Scholar

  • [14] Malygin V.M. 1983. Sistematika obyknovennych polevok [Systematic of common voles]. Nauka, Moscow, 207 pp. Google Scholar

  • [15] Markov G. & Chassovnikarova T. 1999. Epigenetic characteristics and divergence between populations of Apodemus sylvaticus in Bulgaria. Folia Zool. 48(Suppl. 1): 63–67. Google Scholar

  • [16] Markov G. & Gospodinova M. 2005. Bioindikatorna epigenetichna charakteristika na zoomonitora zhltogrla gorska mishka (Apodemus flavicollis) v parkovi teritorii na grad Sofija [Bioindicator epigenetic characteristic of the zoomonitor yellow-necked wood mouse (Apodemus flavicollis) in park territories in Sofia]. Ekologichno inzhenerstvo i opazvane na okolnata sreda [Ecol. Engineer. Environ. Protect.] 3–4: 55–59. Google Scholar

  • [17] Markov G. & Kocheva M. 2007. Craniometric characteristics and diff erentiation of the sibling vole species Microtus arvalis and Microtus rossiaemeriodinalis. Acta Zool. Bulg. 59(2): 145–152. Google Scholar

  • [18] Markov G. & Kocheva M. 2008. Sympatric distribution of the sibling vole species Microtus arvalis and Microtus rossiaemeridionalis (Rodentia, Cricetidae) in Bulgaria. Acta Zool. Bulg. 60(1): 107–111. Google Scholar

  • [19] Markov G., Yigit N., Kocheva M. & Colak E. 2009. A refined method for craniometrical identification of the sibling vole species Microtus arvalis and Microtus rossiameridionalis in Europe and the Asiatic part of Turkey. North-Western Journal of Zoology 5(1): 1–7. Google Scholar

  • [20] Mazeikyte R., Baranauskas K., Morkünas V. & Mickevicius E. 1999. Distribution of the sibling vole (Microtus rossiaemeridionalis Ognev, 1924) (Rodentia, Cricetidae) in Lithuania. Acta Zool. Lith. 9(1): 3–15. DOI: 10.1080/13921657.1999.10512256 http://dx.doi.org/10.1080/13921657.1999.10512256CrossrefGoogle Scholar

  • [21] Meyer M.N., Orlov V.N. & Skholl’ E.D. 1969. Ispoljzovanie dannikh kariologicheskogo, fiziologicheskogo i citologicheskogo analizov dlya videleniya novogo vida u grizunov (Rodentia, Mammalia) [New rodent species (Rodentia, Mammalia) found on the grounds of karyological, physiological and cytophysiological analyses.] Dokl. AN SSSR 188(6): 1411–1414. Google Scholar

  • [22] Saccheri I., Kuussaari M., Kankare M., Vikman P., Fortelius W. & Hanski I. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392: 491–494. DOI: 10.1038/33136 http://dx.doi.org/10.1038/33136CrossrefGoogle Scholar

  • [23] Shenbrot G.I. & Krasnov B.R. 2005. An Atlas of the Geographic Distribution of the Arvicoline Rodents of the World (Rodentia, Muridae, Arvicolinae). Pensoft, Sofia, 350 pp. ISBN: 9546422436 Google Scholar

  • [24] Sjøvold T. 1973. The occurrence of minor, non-metrical variation in the skeleton and their quantitative treatment for population comparison. Homo 24: 204–233. Google Scholar

  • [25] Sjøvold T. 1977. Non-metrical divergence between skeletal populations. The theorical foundation and biological importance of C.A.B. Smith’s Mean mesure of Divergence. Ossa 4(Suppl. 1), 133 pp Google Scholar

  • [26] Smith M.F. 1981 Relationships between genetic variability and niche dimensions among coexisting species of Peromyscus. J. Mamm. 62(2): 273–285. http://dx.doi.org/10.2307/1380704CrossrefGoogle Scholar

  • [27] Sokolov V.E. & Bashenina N.V. (eds) 1994. Obiknovennaya polevka: vidi-dvojniki: Microtus arvalis Pallas, 1779, M. rossiaemeridionalis Ognev, 1924 [Common Vole: The Sibling Species]. Nauka, Moscow, 432 pp. Google Scholar

  • [28] Spitzenberger F., Englisch H., Hammer S., Hartl G.B. & Suchentrunk F. 1999. Morphological and genetic differentiation of bank voles, Clethrionomys glareolus, from the Eastern Alps. Folia Zool. 48(Suppl. 1): 69–94. Google Scholar

  • [29] Statistic for Windows, Release 4.3., StatSoft, 1993. Google Scholar

  • [30] Suchentrunk F., Markov G. & Haiden A. 1998. On gene pool divergence of the two karyotypically distinct sibling vole species Microtus arvalis and M. rossiaemeridionalis (Arvicolidae, Rodentia). Folia Zool. 47(2): 103–114. Google Scholar

  • [31] Tilman D. 1996. Biodiversity: Population versus ecosystem stability. Ecology 77(2): 350–363. DOI: 10.2307/2265614 http://dx.doi.org/10.2307/2265614CrossrefGoogle Scholar

  • [32] Uhlíková J. 2004. Epigenetic and dental variation of the common vole, Microtus arvalis (Mammalia: Rodentia) in the Czech Republic. Folia Zool. 53(2): 157–170. Google Scholar

  • [33] Yiğit N., Kankılıc T. & Colak E. 2007. Reproductive biology and postnatal development of Microtus rossiaemeridionalis Ognev, 1924 (Mammalia: Rodentia) distributed in Turkey. Turk. J. Zool. 31(3): 287–294. Google Scholar

  • [34] Zagorodnyuk I., Henttonen H., Amori G., Hutterer R., Kryštufek B., Yiğit N., Mitsain G. & Munoz L.J.P. 2008. Microtus levis. In: IUCN 2010. IUCN Red List of Threatened Species, version 2010.4. Available at http://www.iucnredlist.org/apps/redlist/details/13454/0 Google Scholar

  • [35] Zima J. 1999. Microtus rossiaemeridionalis, p. 246. In: Mitchell-Jones A.J., Amori G., Bogdanowicz W., Kryštufek B., Reijnders P.J.H., Spitzenberger F., Stubbe M., Thissen J.B.M., Vohralik V. & Zima J. The Atlas of European Mammals. Poyser Natural History series, Academic Press, London, 484 pp. ISBN: 0856611301, 9780856611308 Google Scholar

  • [36] Zima J., Cerveny J., Hrabe V., Kral B. & Sebela M. 1981. On the occurrence of Microtus epiroticus in Romania (Arvicolidae, Rodentia). Folia Zool. 30(2): 139–146. Google Scholar

About the article

Published Online: 2013-11-15

Published in Print: 2014-01-01

Citation Information: Biologia, Volume 69, Issue 1, Pages 101–106, ISSN (Online) 1336-9563, DOI: https://doi.org/10.2478/s11756-013-0288-x.

Export Citation

© 2013 Slovak Academy of Sciences. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Comments (0)

Please log in or register to comment.
Log in