Abstract
Recent water voles (genus Arvicola) display a prominent morphological diversity with a strong ecotypical background but with unclear taxonomic associations. We provide a novel synthetic view on the evolutionary history and the current taxonomic richness in the genus. Our molecular reconstruction, based on a 1143-bp-long sequence of cytochrome b and a 926-bp interphotoreceptor retinoid binding protein (irbp) confirmed the monophyly of four species (amphibius, sapidus, monticola and italicus) recognized thus far, and retrieved a new deeply divergent lineage from West Iran. Genetic divergence of the Iranian lineage (>9.0%) is inside the range of interspecies distances, exceeding the interspecies divergences between the remaining Arvicola species (range, 4.3–8.7%). The oldest name available for the Iranian phylogroup is Arvicola persicus de Filippi, 1865, with the type locality in Soltaniyeh, Iran. The molecular clock suggests the divergence of A. persicus in the Early Pleistocene (2.545 Ma), and the current radiation of the remaining species between 1.535 Ma (Arvicola sapidus) and 0.671 Ma. While A. sapidus possibly evolved from Arvicola jacobaeus, a fossil ancestor to A. persicus is unknown. The aquatic life-style of Mimomys savini, a direct ancestor to some fossil Arvicola, is retained in recent stem species A. sapidus and A. persicus, while a major shift toward fossorial morphotype characterizes the terminal lineages (amphibius, italicus and monticola). We suggest that habitat-dependent morphological plasticity and positive enamel differentiation in Arvicola amphibius widened its ecological niche that might trigger a range expansion across c. 12 million km2, making it one of the largest among arvicolines.
Acknowledgments
AM would like to express his gratefulness to Hamed Hanifi and Mojtaba Karami for their help during the fieldwork. Karolyn Close edited for grammar and style, Georgy Shenbrot helped with the map in Figure 1, and Miloš Anděra granted permission to use his photograph of Arvicola amphibious. This study was funded by grants from the Ferdowsi University of Mashhad (project nos.: 2/37624 to AM) and the Slovenian Research Agency (research core funding no. P1-0255 to BK).
References
Abramson, N.I., V.S. Lebedev, A.S. Tesakov and A.A. Bannikova. 2009. Supraspecies relationships in the subfamily Arvicolinae (Rodentia, Cricetidae): an unexpected result of nuclear gene analysis. Mol. Biol. 43: 834–846.10.1134/S0026893309050148Search in Google Scholar
Avise, J.C. 2000. Phylogeography: the history of formation of species. Harvard University Press, Cambridge.10.2307/j.ctv1nzfgj7Search in Google Scholar
Baker, R.J. and R.D. Bradley. 2006. Speciation in mammals and the genetic species concept. J. Mammal. 87: 643–662.10.1644/06-MAMM-F-038R2.1Search in Google Scholar PubMed PubMed Central
Bannikova, A.A., V.S. Lebedev, A.A. Lissovsky, V. Matrosova, N.I. Abramson, E.V. Obolenskaya and A.S. Tesakov. 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: 595–613.10.1111/j.1095-8312.2009.01378.xSearch in Google Scholar
Bannikova, A.A., A.M. Sighazeva, V.G. Malikov, F.N. Golenishchev and R.I. Dzuev. 2013. Genetic diversity of Chionomys genus (Mammalia, Arvicolinae) and comparative phylogeography of snow voles. Russ. J. Genet. 49: 561–575.10.1134/S1022795413050025Search in Google Scholar
Bannikova, A.A., E.D. Zemlemerova, P. Colangelo, M. Sozen, M. Sevinskim, A.A. Kidov, R.I. Dzuev, B. Kryštufek and V.V. Lebedev. 2015. An underground burst of diversity – a new look at the phylogeny and taxonomy of the genus Talpa Linnaeus, 1758 (Mammalia: Talpidae) as revealed by nuclear and mitochondrial genes. Zool. J. Linn. Soc. 175: 830–948.10.1111/zoj.12298Search in Google Scholar
Barbosa, S., J. Pauperio, J.B. Searle and P.C. Alves. 2013. Genetic identification of Iberian rodent species using both mitochondrial and nuclear loci: application to noninvasive sampling. Mol. Ecol. Resour. 13: 43–56.10.1111/1755-0998.12024Search in Google Scholar PubMed
Baskevich, M.I., S.G. Potapov, L.A. Khlyap, N.M. Okulova, U.M. Ashibokov, M.P. Grigoriev and T.K. Dzagurova. 2015. Chromosomal and molecular investigations of cryptic species of the subgenus Terricola (Rodentia, Arvicolinae, Microtus) in the Caucasian region: analysis of new records. Zool. Zh. 94: 963–971.Search in Google Scholar
Castiglia, R., G. Aloise, G. Amori, F. Annesi, S. Bertolino, D. Capizzi, M. Mori and P. Colangelo. 2016. The Italian peninsula hosts a divergent mtDNA lineage of the water vole, Arvicola amphibius sl, including fossorial and aquatic ecotypes. Hystrix 27: 1–5.Search in Google Scholar
Centeno-Cuadros, A. and J.A. Godoy. 2010. Structure, organization and nucleotide diversity of the mitochondrial control region and cytochrome b of southern water vole (Arvicola sapidus). Mitochondrial DNA 21: 48–53.10.3109/19401731003681103Search in Google Scholar PubMed
Centeno-Cuadros, A., M. Delibes and J.A. Godoy. 2009. Dating the divergence between Southern and European water voles using molecular coalescent-based methods. J. Zool. 279: 404–409.10.1111/j.1469-7998.2009.00632.xSearch in Google Scholar
Chaline, J. 1986. Continental faunal units of the Plio-Pleistocene of France. Mem. Soc. Geo. Ital. 31: 175–183.Search in Google Scholar
Conroy, C.J. and J.A. Cook. 1999. MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. J. Mamm. Evol. 6: 221–245.10.1023/A:1020561623890Search in Google Scholar
Cuenca-Bescós, G. and N. García. 2007. Biostratigraphic succession of the Early and Middle Pleistocene mammal faunas of the Atapuerca cave site (Burgos, Spain). Courier Forschungsinstitut Senckenberg. 259: 99−110.Search in Google Scholar
Cuenca-Bescós, G., J. Agustí, J. Lira, M.M. Rubio and J. Rofes. 2010. A new species of water vole from the early Pleistocene of Southern Europe. Acta Palaeontol. Pol. 55: 565–580.10.4202/app.2009.0027Search in Google Scholar
Darvish, J., Z. Mohammadi, F. Ghorbani, A. Mahmoudi and S. Dubey. 2015. Phylogenetic relationships of Apodemus Kaup, 1829 (Rodentia: Muridae) species in the Eastern Mediterranean inferred from mitochondrial DNA, with emphasis on Iranian species. J. Mamm. Evol. 22: 583–595.10.1007/s10914-015-9294-9Search in Google Scholar
D’Elı́a, G. 2003. Phylogenetics of sigmodontinae (Rodentia, Muroidea, Cricetidae), with special reference to the akodont group, and with additional comments on historical biogeography. Cladistics 19: 307−323.10.1111/j.1096-0031.2003.tb00375.xSearch in Google Scholar
De Filippi, F. 1865. Note di un Viaggio in Persia nel 1862. Volume 1. G. Daelli, Milano. pp. viii+1–396.Search in Google Scholar
Dianat, M., J. Darvish, R. Cornette, M. Aliabadian and V. Nicolas. 2017. Evolutionary history of the Persian Jird, Meriones persicus, based on genetics, species distribution modelling and morphometric data. J. Zool. Syst. Evol. Res. 55: 29–45.10.1111/jzs.12145Search in Google Scholar
Drummond, A.J. and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7: 214.10.1186/1471-2148-7-214Search in Google Scholar PubMed PubMed Central
Drummond, A.J., A. Rambaut and M.A. Suchard. 2015a. Bayesian evolutionary analysis sampling trees v1.8.2. http://beast.bio.ed.ac.uk.Search in Google Scholar
Drummond, A.J., A. Rambaut M.A. Suchard and W. Xie. 2015b. BEAUti v1.8.2: Bayesian evolutionary analysis utility. http://beast.bio.ed.ac.uk.Search in Google Scholar
Ellerman, J.R. and T.C.S. Morrison-Scott. 1951. Checklist of Palaearctic and Indian mammals 1758 to 1946. Trustees of the British Museum (Natural History), London. p. 810.Search in Google Scholar
Fejfar, O., W.D. Heinrich and E.H. Lindsay. 1998. Updating the Neogene Rodent biochronology in Europe. Mededelingen Nederlands Instituut voor Geowetenschappen TNO 60: 533–554.Search in Google Scholar
Fejfar, O., W.D. Heinrich, L. Kordos and L.C. Maul. 2011. Microtoid cricetids and the early history of arvicolids (Mammalia: Rodentia). Palaeontol. Electron. 14.Search in Google Scholar
Fink, S., M.C. Fischer, L. Excoffier and G. Heckel. 2010. Genomic scans support repetitive continental colonization events during the rapid radiation of voles (Rodentia: Microtus): the utility of AFLPs versus mitochondrial and nuclear sequence markers. Syst. Biol. 59: 548–572.10.1093/sysbio/syq042Search in Google Scholar PubMed
Fisher-Reid, M.C. and J.J. Wiens. 2011. What are the consequences of combining nuclear and mitochondrial data for phylogenetic analysis? Lessons from Plethodon salamanders and 13 other vertebrate clades. BMC Evol. Biol. 11: 300.10.1186/1471-2148-11-300Search in Google Scholar PubMed PubMed Central
Galewski, T., M. Tilak, S. Sanche, P. Chevret, E. Paradis and E.J.P. Douzery, 2006. The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evol. Biol. 6: 80.10.1186/1471-2148-6-80Search in Google Scholar PubMed PubMed Central
Garapich, A. and A. Nadachowski. 1996. A contribution to the origin of Allophaiomys (Arvicolidae, Rodentia) in Central Europe: the relationship between Mimomys and Allophaiomys from Kamyk (Poland). Acta Zool. Cracov. 39: 179–184.Search in Google Scholar
Guindon, S., J.F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk and O. Gascuel. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59: 307–321.10.1093/sysbio/syq010Search in Google Scholar PubMed
Harrison, R.G. and E.L. Larson. 2014. Hybridization, introgression, and the nature of species boundaries. J. Hered. 105(S1): 795–809.10.1093/jhered/esu033Search in Google Scholar PubMed
Haynes, S., M. Jaarola and J.B. Searle. 2003. Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago. Mol. Ecol. 12: 951–956.10.1046/j.1365-294X.2003.01795.xSearch in Google Scholar PubMed
Heinrich, W.-D. 1978. Zur biometrischen Erfassung eines Evolutionstrends bei Arvicola (Rodentia, Mammalia) aus dem Pleistozän Thüringens. Säugetierkundliche Informationen 2: 3–21.Search in Google Scholar
Hewitt, G.M. 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.10.1038/35016000Search in Google Scholar PubMed
Hinton, M.A.C. 1926. Monograph of the voles and lemmings (Microtinae) living and extinct. Vol. 1. British Museum, Natural History, London. 488 pp.+15 plates.10.5962/bhl.title.8319Search in Google Scholar
Hope, A.G., E. Waltari, D.C. Payer, J.A. Cook and S.L. Talbot. 2013. Future distribution of tundra refugia in northern Alaska. Nat. Clim. Change 3: 931.10.1038/nclimate1926Search in Google Scholar
Horáček, I. and V. Ložek. 1988. Palaeozoology and the mid-European Quaternary past: scope of the approach and selected results. – Rozpravy Československé Akademie Věd, Řada Matematických a Přírodních Věd. 98: 1–102.Search in Google Scholar
Irwin, D., M. Kocher, T.D. and A.C. Wilson. 1991. Evolution of the cytochromeb gene of mammals. J. Mol. Evol. 32: 128–144.10.1007/BF02515385Search in Google Scholar PubMed
Jaarola, M. and J.B. Searle. 2002. Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Mol. Ecol. 11: 2613–2621.10.1046/j.1365-294X.2002.01639.xSearch in Google Scholar
Jaarola, M., N. Martínková, I. Gündüz, C. Brunhoff, J. Zima, A. Nadachowski, G. Amori, N.S. Bulatova, B. Chondropoulos, S. Fraguedakis-Tsolis, J. González-Esteban, M.J. López-Fuster, A.S. Kandaurov, H. Kefelioğlu, M. da Luz Mathias, I. Villate and J.B. Searle. 2004. Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol. Phylogenet. Evol. 33: 647–663.10.1016/j.ympev.2004.07.015Search in Google Scholar PubMed
Jánossy, D. 1962. Az első fosszilis vizilóleletek hazánk pleisztocénjéből. [Der erste Nachweis von Hippopotamus antiquus Desmarest im ungarischen Altpleistozän]. Állattani Közlemények 49: 63–74.Search in Google Scholar
Jánossy, D. and A.J. van der Meulen 1975. On Mimomys (Rodentia) from Osztramos-3, North Hungary. Koninklijke Nederlandse Akademie van Wetenschapen, Proceedings, Series B 78: 381–391.Search in Google Scholar
Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.10.1007/BF01731581Search in Google Scholar PubMed
Koenigswald, W.V. 1973. Veränderungen in der Kleinsäugerfauna von Mitteleuropa zwischen Cromer und Eem (Pleistozän). Eiszeitalter und Gegenwart 23/24: 159–167.10.3285/eg.23-24.1.14Search in Google Scholar
Koenigswald, W.V. 1980. Schmelzstruktur und Morphologie in den Molaren der Arvicolidae (Rodentia). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 539: 1–129.Search in Google Scholar
Koenigswald, W.V. and T. van Kolfschoten. 1996. The Mimomys-Arvicola boundary and the enamel thickness quotient (SDQ) of Arvicola as stratigraphic markers in the Middle Pleistocene. In: (Turner, C., ed.), The early Middle Pleistocene in Europe. A.A. Balkema, Rotterdam. pp. 211–226.10.1201/9781003077879-15Search in Google Scholar
Kretzoi, M. 1954. Bericht über die Calabrische (Villafranchische) Fauna von Kisláng, Kom. Fejér. Földtani Intezet Evi Jelentes 1953: 213–264.Search in Google Scholar
Kretzoi, M. 1965. Die Nager und Lagomorphen von Voigtstedt in Thüringen und ihre chronologische Aussage. Paläontologische Abhandlungen, Abteilung A 2: 585–661.Search in Google Scholar
Kretzoi, M. 1969. Skizze einer Arvicoliden-Phylogenie – Stand 1969. Vertebrata Hungarica 11: 155–193.Search in Google Scholar
Kryštufek, B., T. Koren, S. Engelberger, G.F. Horvath, J.J. Purger, A. Arslan, G. Chişamera and D. Murariu. 2015. Fossorial morphotype does not make a species in water voles. Mammalia 79: 293–303.10.1515/mammalia-2014-0059Search in Google Scholar
Kumar, S., G. Stecher and K. Tamura. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874.10.1093/molbev/msw054Search in Google Scholar PubMed PubMed Central
Lv, X., L. Xia, D. Ge, Y. Wu and Q. Yang. 2016. Climatic niche conservatism and ecological opportunity in the explosive radiation of arvicoline rodents (Arvicolinae, Cricetidae). Evolution 70: 1094–1104.10.1111/evo.12919Search in Google Scholar PubMed
Mahmoudi, A., J. Darvish, M. Aliabadian, F.Y. Moghaddam and B. Kryštufek. 2017. New insight into the cradle of the grey voles (subgenus Microtus) inferred from mitochondrial cytochrome b sequences. Mammalia 81: 583–593.10.1515/mammalia-2016-0001Search in Google Scholar
Mahmoudi, A., J. Darvish, R. Siahsarvie, S. Dubey and B. Kryštufek. 2018. Mitochondrial sequences retrieve an ancient lineage of bicolored shrew in the Hyrcanian refugium. Mamm. Biol. 95: 160–163.10.1016/j.mambio.2018.06.006Search in Google Scholar
Martin, Y., G. Gerlach, C. Schlötterer and A. Meyer. 2000. Molecular phylogeny of European muroid rodents based on complete cytochrome b sequences. Mol. Phylogenet. Evol. 16: 37–47.10.1006/mpev.1999.0760Search in Google Scholar PubMed
Masini, F., L.C. Maul, L. Abbazzi and D. Petruso. 2007. New Data on the Morphological Variation of Extant and Fossil European Populations of Arvicola (Rodentia). Hystrix 1: 125.Search in Google Scholar
Maul, L.C. and A.K. Markova. 2007. Similarity and regional differences in Quaternary arvicolid evolution in Central and Eastern Europe. Quat. Int. 160: 81–99.10.1016/j.quaint.2006.09.010Search in Google Scholar
Maul, L.C., F. Masini, L. Abbazzi and A. Turner. 1998. The use of different morphometric data for absolute age calibration of some South and Middle European arvicolid populations. Palaeontogr. Ital. 85: 111–151.Search in Google Scholar
Maul, L.C., F. Masini, S.A. Parfitt, L.I. Rekovets, A. Savorelli. 2014. Evolutionary trends in arvicolids and the endemic murid Mikrotia – new data and a critical overview. Quat. Sci. Rev. 96: 240–258.10.1016/j.quascirev.2013.09.017Search in Google Scholar
McWilliam, H., W. Li, M. Uludag, S. Squizzato, Y.M. Park, N. Buso, A.P. Cowley and R. Lopez. 2013. Analysis tool web services from the EMBL-EBI. Nucleic Acids Res. 41, W597–W600.10.1093/nar/gkt376Search in Google Scholar PubMed PubMed Central
Mendes, F.K., Y. Hahn and M.W. Hahn. 2016. Gene tree discordance can generate patterns of diminishing convergence over time. Mol. Biol. Evol. 33: 3299–3307.10.1093/molbev/msw197Search in Google Scholar PubMed
Miller, G.S. 1896. The genera and subgenera of voles and lemmings. North Am. Fauna 12: 1–85.10.3996/nafa.12.0001Search in Google Scholar
Miller, G.S. 1912. Catalogue of the mammals of Western Europe (Europe exclusive of Russia) in the collection of the British Museum. British Museum, London. pp. 1–1019.10.5962/bhl.title.8345Search in Google Scholar
Musser, G.G. and M.D. Carleton. 2005. Superfamily Muroidea. In: (Wilson, D.E. and D.M. Reeder, eds.) Mammal species of the world: a taxonomic and geographic reference. John Hopkins Univ. Press, Baltimore. pp. 894–1531.Search in Google Scholar
Nadachowski, A. 1991. Systematics, geographic variation, and evolution of snow voles (Chionomys) based on dental characters. Acta Therio. 36: 1–45.10.4098/AT.arch.91-1Search in Google Scholar
Naderi, G., M. Kaboli, M. Karami, M.R. Rezaei, M. Lahoot, M. Kamran, T. Koren and B. Kryštufek. 2013. Mammary number and litter size of the fat dormouse in the southern Caspian coast. Mammalia 78: 335–338.10.1515/mammalia-2013-0069Search in Google Scholar
Newton, E.T. 1881. IV. Notes on the Vertebrata of the Pre-Glacial Forest Bed Series of the East of England. Geological Magazine, N.S., Decade II. 8: 256–259.10.1017/S0016756800117133Search in Google Scholar
Panteleyev, P.A. 2001. The water vole. Mode of the species. Nauka, Moscow. pp. 148–156 [in Russian, titles also in English].Search in Google Scholar
Pardiñas, U.F.J., P. Myers, L. León-Paniagua, N. Ordoñez-Garza, J.A. Cook, B. Kryštufek, R. Haslauer, R. Bradley, G. Shenbrot, and J.L. Patton. 2017. Family Cricetidae (True Hamsters, Voles, Lemmings and New World Rats and Mice). In: (Wilson, D.E., T.E. Lacher Jr. and R.A. Mittermeier, eds.) Handbook of the Mammals of the World. Vol. 7. Rodents II. Lynx Edicions, Barcelona.Search in Google Scholar
Pevzner, M., A.S. Tesakov and E.A. Vangengeim. 1998. The position of the Tizdar locality (Taman Peninsula, Russia) in the magnetochronological scale. Paludicola 2: 95–97.Search in Google Scholar
Pfunder, M., O. Holzgang and J.E. Frey. 2004. Development of microarray-based diagnostics of voles and shrews for use in biodiversity monitoring studies, and evaluation of mitochondrial cytochrome oxidase I vs. cytochrome b as genetic markers. Mol. Ecol. 13: 1277–1286.10.1111/j.1365-294X.2004.02126.xSearch in Google Scholar PubMed
Posada, D. and K.A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.10.1093/bioinformatics/14.9.817Search in Google Scholar PubMed
Rabeder, G. 1981. Die Arvicoliden (Rodentia, Mammalia) aus dem Pliozän und dem älteren Pleistozän von Niederösterreich. Beiträge zur Paläontologie von Österreich 8: 1–373.Search in Google Scholar
Rabeder, G. 1986. Origin and early evolution of the genus Microtus (Arvicolidae, Rodentia). Zeitschrift für Säugetierkunde 51: 350–367.Search in Google Scholar
Robovsky, J., V. Ričankova and J. Zrzavy. 2008. Phylogeny of Arvicolinae (Mammalia, Cricetidae): utility of morphological and molecular data sets in a recently radiating clade. Zool. Scripta 37: 571–590.10.1111/j.1463-6409.2008.00342.xSearch in Google Scholar
Ronquist, F., M. Teslenko, P. Van der Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard and J.P. Huelsenbeck. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542.10.1093/sysbio/sys029Search in Google Scholar PubMed PubMed Central
Röttger, U. 1987. Schmelzbandbreiten an Molaren von Schermäusen (Arvicola Lacepede, 1799). Bonn. Zool. Beitr. 38: 95–105.Search in Google Scholar
Sánchez-Gracia, A. and J. Castresana. 2012. Impact of deep coalescence on the reliability of species tree inference from different types of DNA markers in mammals. PLoS One 7: e30239.10.1371/journal.pone.0030239Search in Google Scholar PubMed PubMed Central
Schlegel, M., H.S. Ali, N. Stieger, M.H. Groschup, R. Wolf and R.G. Ulrich. 2012a. Molecular identification of small mammal species using novel cytochrome B gene-derived degenerated primers. Biochem. Genet. 50: 440–447.10.1007/s10528-011-9487-8Search in Google Scholar PubMed
Schlegel, M., E. Kindler, S.S. Essbauer, R. Wolf, J. Thiel, M.H. Groschup, G. Heckel, R.M. Oehme and R.G. Ulrich. 2012b. Tula virus infections in the Eurasian water vole in Central Europe. Vector Borne Zoonotic Dis. 12: 503–513.10.1089/vbz.2011.0784Search in Google Scholar PubMed
Shenbrot, G.I. and B.R. Krasnov. 2005. Atlas of the geographic distribution of the arvicoline rodents of the world (Rodentia, Muridae: Arvicolinae). Pensoft.Search in Google Scholar
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.10.1093/bioinformatics/btu033Search in Google Scholar PubMed PubMed Central
Stewart, J.R., A.M. Lister, I. Barnes and L. Dalen. 2010. Refugia revisited: individualistic responses of species in space and time. Proc. R. Soc. B 277: 661–671.10.1098/rspb.2009.1272Search in Google Scholar PubMed PubMed Central
Taberlet, P., L. Fumagalli, A.G. Wust-Saucy and J.F. Cosson. 1998. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7: 453–464.10.1046/j.1365-294x.1998.00289.xSearch in Google Scholar PubMed
Thomas, O. 1907. On Mammals from Northern Persia, presented to the National Museum by Col. A. C. Bailward. The Annals and Magazine of Natural History, including zoology, botany and mineralogy, 7th ser. 20: 196–202.10.1080/00222930709487323Search in Google Scholar
Tougard, C. 2017. Did the quaternary climatic fluctuations really influence the tempo and mode of diversification in European rodents? J. Zool. Syst. Evol. Res. 55: 46–56.10.1111/jzs.12152Search in Google Scholar
Wolff, J.O. and R.D. Guthrie. 1985. Why are aquatics mammal so large? Oikos 45: 365–373.10.2307/3565572Search in Google Scholar
Wust Saucy, A.G. 1998. Polymorphisme genetique et phylogeographie du campagnol terrestre Arvicola terrestris. Unpublished PhD Thesis, Faculte des sciences de Lausanne. Université de Neuchatel, Lausanne. Available online at: https://scholar.google.com/scholar?lookup=0&q=Polymorphisme+genetique+et+phylogeographie+du+campagnol+terrestre+Arvicola+terrestris.+Unpublished+PhD+Thesis,+Faculte+des+sciences+de+Lausanne&hl=en&as_sdt=0,5.Search in Google Scholar
Yannic, G., R. Burri, V.G. Malikov and P. Vogel. 2012. Systematics of snow voles (Chionomys, Arvicolinae) revisited. Mol. Phylogenet. Evol. 62: 806–815.10.1016/j.ympev.2011.12.004Search in Google Scholar PubMed
Zink, R.M. and G.F. Barrowclough. 2008. Mitochondrial DNA under siege in avian phylogeography. Mol. Ecol. 17: 2107–2121.10.1111/j.1365-294X.2008.03737.xSearch in Google Scholar PubMed
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