Sympatric area of Myodes glareolus and M. rutilus (Rodentia, Cricetidae): historic and recent hybridization

E.N. Melnikova (Rodchenkova), I.A. Kshnyasev, S.Yu. Bodrov, S.V. Mukhacheva, Yu.A. Davydova and N.I. Abramson

Proceedings of the Zoological Institute RAS, 2012, 316(4): 307–323 · https://doi.org/10.31610/trudyzin/2012.316.4.307

Full text

Abstract

The bank vole (Myodes glareolus) and the northern red-backed vole (M. rutilus) are two phylogenetically close sylvatic species with a widely sympatric range (European part of Russia, Western Siberia). A significant number of M. glareolus with mitochondrial genome of M. rutilus was detected in this sympatry zone earlier and only one of the first generation hybrid (F1) was discovered. The aim of the present study is to assess the extent of modern hybridization and to analyze the possible conditions of interspecies hybridization between the voles. The cytochrome b gene sequences of M. glareolus (164) and M. rutilus (108) sampled in the sympatric area were studied. In order to identify the modern hybrids, 841 individuals of M. glareolus were analyzed with cytochrome b PCR-typing, two microsatellite loci and one nuclear gene (LCAT). The detected unique case of the hybridization between M. glareolus and M. rutilus in nature is evidence that it is a possible at present but rare event. According to findings in the Urals M. glareolus populations, the chances of modern hybridization in the depression phases were higher than those regardless of cycle phase. Interspecific hybridization between these vole species in the historical past may have occurred in the southern Urals refuge during the Last Glacial Maximum, at a low density of both species. A mass independent hybridization during the formation of the sympatry seems less likely.

Key words

hybridization, mitochondrial DNA introgression, Myodes, Rodentia, sympatric range

Submitted June 27, 2012 · Accepted November 13, 2012 · Published December 25, 2012

References

Abramson N.I. and Bodrov S.Yu. 2008. Genetic differentiation and phylogeography of Clethrionomys rutilus Pallas 1811 inferred from variation of mitochondrial cytochrome b gene. Abstract of 11th International Conference on Rodent Biology, Rodens et Spatium, Myshkin, 64 p.

Abramson N.I., Lebedev V.S., Tesakov A.S. and Bannikova A.A. 2009a. Supraspecies relationships in the subfamily Arvicolinae (Rodentia, Cricetidae): an unexpected result of nuclear gene analysis. Molecular Biology, 43: 834–846. https://doi.org/10.1134/S0026893309050148

Abramson N.I., Rodchenkova E.N. and Kostygov A.Yu. 2009b. Genetic variation and phylogeography of the bank vole (Clethrionomys glareolus, Arvicolinae, Rodentia) in Russia with special reference to the introgression of the mtDNA of a closely related species, red-backed vole (C. rutilus). Russian Journal of Genetics, 45(5): 535–547. https://doi.org/10.1134/S1022795409050044

Abramson N.I., Rodchenkova E.N., Fokin M.V., Rakitin S.B. and Gileva E.A. 2009c. Recent and ancient introgression of mitochondrial DNA between the red (Clethrionomys rutilus) and bank (Clethrionomys glareolus) voles (Rodentia, Cricetidae). Doklady Biological Sciences, 425: 147–150. https://doi.org/10.1134/S0012496609020185

Bandelt H-J., Forster P. and Rohl A. 1999. Median-joining networks for inferring intraspeciﬁc phylogenies. Molecular Biology and Evolution, 16: 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

Barker F.S., Helyar S.J. and Kemp S.J. 2005. Highly polymorphic microsatellite loci in the bank vole (Clethrionomys glareolus). Molecular Ecology Notes, 5: 311–313. https://doi.org/10.1111/j.1471-8286.2005.00911.x

Bashenina N.V. (Ed.) 1981. Yevropeyskaya ryzhaya polevka [bank vole]. Nauka, Moscow, 352 p. [In Russian].

Borodin A.V., Davydova Yu.A. and Fominykh M.A. 2011. A natural hybrid between the red (Clethrionomys rutilus) and the bank (Clethrionomys glareolus) vole (Arvicolinae, Rodentia,) in the middle Urals. Zoological Journal, 5: 634–640. [In Russian].

Brunhoff C., Galbreath K.E., Fedorov V.B., Cook J.A. and Jaarola M. 2003. Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes. Molecular Ecology, 12: 957–968. https://doi.org/10.1046/j.1365-294X.2003.01796.x

Dekonenko A., Yakimenko V., Ivanov A., Morozov V., Nikitin P., Khasanova S., Dzagurova T., Tkachenko E. and Schmaljohn C. 2003. Genetic similarity of puumala viruses found in Finland and western Siberia and of the mitochondrial DNA of their rodent hosts suggests a common evolutionary origin. Infection, Genetics and Evolution, 3: 245–247. https://doi.org/10.1016/S1567-1348(03)00088-1

Deffontaine V., Libois R., Kotlik P., Sommer R., Nieberding C., Paradis E., Searle J.B. and Michaux J.R. 2005. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Molecular Ecology, 14: 1727–1739. https://doi.org/10.1111/j.1365-294X.2005.02506.x

Excoffier L. 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology, 13: 853–864. https://doi.org/10.1046/j.1365-294X.2003.02004.x

Excoffier L., G. Laval and Schneider S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1: 47–50. https://doi.org/10.1177/117693430500100003

Fu Y.X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147: 915–925. https://doi.org/10.1093/genetics/147.2.915

Gockel J., Harr B., Schlötterer C., Arnold W., Gerlach G. and Tautz D. 1997. Isolation and characterization of microsatellite loci from Apodemus flavicollis (Rodentia, Muridae) and Clethrionomys glareolus (Rodentia, Cricetidae). Molecular Ecology, 6: 597–599. https://doi.org/10.1046/j.1365-294X.1997.00222.x

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment, editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series, 41: 95–98.

Jaarola M. and Searle J.B. 2002. Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Molecular Ecology, 11: 2613–2621. https://doi.org/10.1046/j.1365-294X.2002.01639.x

Jaarola M., Tegelström H. and Fredga K. 1999. Colonization history in Fennoscandian rodents. Biological Journal of the Linnean Society, 68: 113–127. https://doi.org/10.1111/j.1095-8312.1999.tb01161.x

Kshnyasev I.A., Davydova Yu.A. and Maklakov K.V. 2011. Populyatsyonye tsikly lesnykh polevok v yuzhnoy tayge: scenariy dinamiki “khishchnik–zhertva” [Voles’ population cycles in the southern taiga: the scenario of “predator-prey” dynamics]. Proceeding of the second national conference of mathematical modeling in ecology, Pushino, ISSP. Academy of Sciences, 145–146. [In Russian].

Kshnyasev I.A. and Marin Y. 2012. Taiga rodent community before and after environmental disturbances caused by wind storm tree fall and wild fire. The 13th Rodens et Spatium Conference – Abstracts. 52 p.

Markova A.K. and Kolfschoten T. van (Eds.) 2008. Evolutsiya ekosistem Yevropy pri perekhode ot pleystotsena k golotsenu (24-8 tus. l.n.) [Evolution of the European Ecosystems during Pleistocene–Holocene Transition (24-8 kyr BP)]. KMK, Moscow, 556 p. [In Russian].

Markova A.K., Smirnov N.G., Kozharinov A.V., Kazantseva N.E., Simakova A.N. and Kitaev L.M. 1995. Late Pleistocene distribution and diversity of mammals in northern Eurasia (paleofauna Database). Paleontologia i Evolucio. 28/29: 5–143.

Miller S.A., Dykes D.D. and Polesky H.F. 1988. A simple salting out procedure for extraction DNA from human nucleated cells. Nucleic Acids Research, 16: 12–15. https://doi.org/10.1093/nar/16.3.1215

Mukhacheva S.V., Davydova Yu.A. and Kshnyasev I.A. 2010. Responses of small mammal community to environmental pollution by emissions from copper smelter. Russian Journal of Ecology, 41: 513–518. https://doi.org/10.1134/S1067413610060081

Nei M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, 512 p. https://doi.org/10.7312/nei-92038

Newton I. 2003. The speciation and biogeography of birds. Academic Press, 668 p.

Osipova O.V. and Soktin A.A. 2008. Experimental simulation of ancient hybridization between bank and red vole. Doklady Biological Sciences, 420: 169–171. https://doi.org/10.1134/S0012496608030083

Potapov S.G., Illarionova N.A., Andreeva T.A., Baskevich M.I., Okulova N.M., Lavrenchenko L.A. and Orlov V.N. 2007. Transfer of mitochondrial genome of the northern red backed vole (Clethrionomys rutilus) to the bank vole (C. glareolus) in North Western Europe. Doklady Biological Sciences, 417: 435–438. https://doi.org/10.1134/S0012496607060075

Rogers A.R. and Harpending H. 1992. Population growth makes waves in the distribution of pairwise differences. Molecular Biology and Evolution, 9: 552–569.

Rozas J., Sánchez-DelBarrio J.C., Messeguer X. and Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19: 2496–2497. https://doi.org/10.1093/bioinformatics/btg359

Schneider S. and Excoffier L. 1999. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics, 152: 1079–1089. https://doi.org/10.1093/genetics/152.3.1079

Selander R.K. 1971. Species and speciation in birds. In: D.S. Farner and J.R. King (Eds.). Avian Biology, 1: 57–147.

Semerikov V.L. and Lascoux M. 2003. Nuclear and cytoplasmic variation within and between Eurasian Larix (Pinaceae) species. American Journal of Botany, 90(8): 1113–1123. https://doi.org/10.3732/ajb.90.8.1113

Shenbrot G.I. and Krasnov B.R. 2005. An atlas of the geographic distribution of the arvicoline rodents of the world (Rodentia, Muridae: Arvicolinae). Pensoft, Sofia–Moscow, 336 p.

Slatkin M. and Hudson R.R. 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129: 555–562. https://doi.org/10.1093/genetics/129.2.555

StatSoft 2007. STATISTICA (data analysis software system), version 6.0. www.statsoft.com

Stenseth N.C. and Gustafsson T.O. 1985. Reproductive rates, survival, dispersal and cyclicity in Clethrionomys species: Some theoretical considerations. Annales Zoologici Fennici, 22: 289–301.

Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123: 585–595. https://doi.org/10.1093/genetics/123.3.585

Tajima F. 1993. Measurement of DNA polymorphism. In: N. Takahata and A.G. Clark (Eds.). Mechanisms of Molecular Evolution. Sinauer Associates, Sunderland, MA: 37–59.

Tegelström H. 1987. Transfer of mitochondrial DNA from the northern red-backed vole (Clethrionomys rutilus) to the bank vole bank vole (C. glareolus). Journal of Molecular Evolution, 24: 218–227. https://doi.org/10.1007/BF02111235

Thompson J.D., Higgins D.G. and Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22: 4673–4680. https://doi.org/10.1093/nar/22.22.4673

Valiranta M., Kaakinen A., Kuhry P., Kultti S., Salonen J.S. and Seppa H. 2011. Scattered late-glacial and early Holocene tree populations as dispersal nuclei for forest development in north-eastern European Russia. Journal of Biogeography, 38: 922–932. https://doi.org/10.1111/j.1365-2699.2010.02448.x

Velichko A.A. (Ed.) 2009. Paleoklimaty i paleolandshafty vnetropicheskogo prostranstva Severnogo polushariya. Pozdniy pleystotsen-golotsen Atlas-monograph. [Paleoclimates and paleoenvironments of extra-tropical area of the Northern Hemisphere. Late Pleistocene – Holocene. Atlas-monograph]. GEOS, Moscow, 129 p. [In Russian].

Wójcik J.M., Kawałko A., Marková S., Searle J.B. and Kotlík P. 2010. Phylogeographic signatures of northward post-glacial colonization from high-latitude refugia: a case study of bank voles using museum specimens. Journal of Zoology, 281: 249–262. https://doi.org/10.1111/j.1469-7998.2010.00699.x