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Supraspecies relationships in the subfamily Arvicolinae (Rodentia, Cricetidae): An unexpected result of nuclear gene analysis

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Abstract

Phylogenetic analysis of the supraspecies relationships was carried out using partial sequences of two nuclear genes in the subfamily Arvicolinae, which is one of the youngest and species-rich groups of myomorph rodents. The analysis with the new data resolved the majority of polytomy nodes in the phylogenetic trees reported for Arvicolinae, suggesting a gradual, rather than a saltatory, mode for their evolution. Mole voles Ellobiusini, steppe voles Lagurini, and gray voles Arvicolini were fount to be a monophyletic group that corresponds to the latest third wave of radiation within the subfamily. Red-back voles Myodini (=Clethrionomini) are a sister clade to this group and correspond to the second radiation wave. The order of divergence remained unresolved for the earliest radiation wave (Ondatrini, Prometheomyini, Dicrostonychini, and Lemmini). The close relationships observed for mole, gray, and steppe voles are unexpected and contradict the conventional views that Ellobiusini are an ancient group and are separate from all other voles on evidence of the extreme simplicity of their rooted molars and the peculiar structure of their skull and postcranial skeleton. It was assumed that many of these morphological characters indicate adaptation to subterranean life and provide no phylogenetic signal.

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References

  1. Zazhigin V.S. 1980. Gryzuny pozdnego pliotsena i antropogena yuga Zapadnoi Sibiri (Late Ploicene and Anthropogene Rodents in the South of Western Siberia). Moscow: Nauka.

    Google Scholar 

  2. Nesin V.a. 1996. The Most Ancient Fossil Vole (Rodentia, Cricetidae) From The Lower Pontic Of Southern Ukraine. Vestn. Zool. 3, 74–75.

    Google Scholar 

  3. Topachevskii, V.A. and Skorik, A.F., 1977. Gryzuny rannetamanskoi fauny tiligul’skogo razreza (Rodents of the Early Taman Fauna from the Tiligul Pit). Kiev: Naukova Dumka.

    Google Scholar 

  4. Erbaeva M.A. 1970. Istoriya antropogenovoi fauny zaitseobraznykh i gryzunov Selenginskogo srednegor’ya (History of the Anthropogenic Lagomorph and Rodent Fauna of the Selenga Middle Mountain Region). Moscow: Nauka.

    Google Scholar 

  5. Gromov I.M. Polyakov I.Ya., 1977. Fauna SSSR. Mlekopitayushchie (The USSR Fauna: Mammals), vol. 3, issue 8. Leningrad: Nauka.

    Google Scholar 

  6. Repenning C.A., Grady F.M. 1988. The microtine rodents of the Cheetah Room Fauna, Hamilton Cave, West Virginia, and the spontaneous origin of Synaptomys. United States Geological Survey Bulletin. 1853, 1–32.

    Google Scholar 

  7. Kowalski K. 2001. Pleistocene rodents of Europe. Folia Quaternaria. 72, 1–389.

    Google Scholar 

  8. Hinton M.A.C. 1926. Monograph of voles and lemmings (Microtinae) living and extinct. London: British Museum (Natural History).

    Google Scholar 

  9. Kretzoi M. 1969. Skizze einer Arvicoliden Phylogenie-Stand. Vert. Hung. Mus. Hist.-Nat. Hung. 11, 155–192.

    Google Scholar 

  10. Gromov I.M. 1972. Supraspecific taxonomic categories in the vole subfamily, Microtinae, and their probable kinship connections. Sb. Tr. Zool. Muz. Mosk. Gos. Univ. 13, 8–32.

    Google Scholar 

  11. Agajanyan A.K., Yatsenko V.N. 1984. Phylogenetic relationships of North Eurasian voles. In: Problemy izmenchivosti i filogenii mlekopitayushchikh (Problems in Mammal Variation and Phylogeny), Moscow: Mosk. Gos. Univ., pp. 135–190.

    Google Scholar 

  12. Zagorodnyuk I.V. 1990. Karyotypic variation and taxonomy of gray voles (Rodentia, Arvicolini): 1. Species composition and chromosome numbers. Vestn. Zool. 2, 26–37.

    Google Scholar 

  13. Modi W.S. 1987. Phylogenetic analyses of chromosomal banding patterns among the Nearctic Arvicolidae (Mammalia: Rodentia). Syst. Zool. 36, 109–136.

    Article  Google Scholar 

  14. Mezhzherin S.V., Morozov-Leonov S.Yu., Kuznetsova I.A., 1995. Biochemical variation and genetic divergence of palearctic voles (Arvicolidae): Subgenus Terricola and genera Lemmus Link 1795, Dicrostonyx Gloger 1841, Lagurus Gloger 1842, and Ellobius Fischer von Waldheim 1814. Genetika (Moscow). 31, 788–797.

    PubMed  CAS  Google Scholar 

  15. Chaline J., Graf J.-D. 1988. Phylogeny of the Arvicolidae (Rodentia): biochemical and paleontological evidence. J. Mammal. 69, 22–33.

    Article  Google Scholar 

  16. Modi W.S. 1996. Phylogenetic history of LINE-1 among arvicolid rodents. Mol. Biol. Evol. 13, 633–641.

    PubMed  CAS  Google Scholar 

  17. Conroy C.J., Cook J.A. 1999. MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. J. Mammal. Evol. 6, 221–245.

    Article  Google Scholar 

  18. Galewski T., Tilak M., Sanchez S., Chevret P., Paradis E., Douzery E.J.P. 2006. The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evol. Biol. 6, 1–17.

    Article  Google Scholar 

  19. Buzan E., Krustufek B., Hanfling B., Hutchinson W. 2008. Mitochondrial phylogeny of Arvicolinae using comprehensive taxonomic sampling yields new insights. Biol. J. Linnean Soc. 94, 825–835.

    Article  Google Scholar 

  20. Hooper E.T., Hart B. 1962. A synopsis of recent North American microtine rodents. Miscellaneous publications. Museum Zoology, University of Michigan. 120, 1–68.

    Google Scholar 

  21. McKenna M.C., Bell S.K. 1997. Classification of mammals above the species level. N.Y.: Columbia Univ. Press.

    Google Scholar 

  22. Martin Y., Gerlach G., Schlotterer C., Meyer A. 2000. Molecular phylogeny of European muroid rodents based on complete cytochrome b sequences. Mol. Phylogen. Evol. 1, 37–47.

    Article  Google Scholar 

  23. Musser G.G., Carleton M.D. 2005. Superfamily Muroidea. In: Mammal species of the world. A taxonomic and geographic reference. Eds Wilson D.E., Reeder D.-A.M. 3rd edn. V. 2. Baltimore, MD: John Hopkins Univ. Press, 894–1531.

    Google Scholar 

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

    Google Scholar 

  25. Jaarola M., Martinkova N., Gunduz I., Brunhoff C., Zima J., Nadachowski A., Amori G., Bulatova N.S., Chondropoulos B., Fraguedakis-Tsolis S., Gonzalez-Esteban J., Lopez-Fuster M.J., Kandaurov A.S., Kefelioglu H., Mathias M.D., Villate I., Searle J.B. 2004. Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol. Phylogen. Evol. 33, 647–663.

    Article  CAS  Google Scholar 

  26. Springer M.S., DeBry R.W., Douady C., Amrine H.M., Madsen O., de Jong W.W, Stanhope M.J. 2001. Mitochondrial versus nuclear gene sequences in deep-level mammalian phylogeny reconstruction. Mol. Biol. Evol. 18, 132–143.

    PubMed  CAS  Google Scholar 

  27. Halanych K.M., Robinson T.J. 1999. Multiple substitutions affect the phylogenetic utility of cytochrome b and 12S rDNA data: Examining a rapid radiation in leporid (Lagomorpha) evolution. J. Mol. Evol. 48, 369–379.

    Article  PubMed  CAS  Google Scholar 

  28. Michaux J., Catzfelius F. 2000. The bushlike radiation of muroid Rodents is exemplified by the molecular phylogeny of the LCAT nuclear gene. Mol. Phylogen. Evol. 17, 280–293.

    Article  CAS  Google Scholar 

  29. Robinson M., Catzeflis F., Briolay J., Mouchiroud D. 1997. Molecular phylogeny of rodents, with special emphasis on murids: evidence from nuclear gene LCAT. Mol. Phylogenet. Evol. 8, 423–434.

    Article  PubMed  CAS  Google Scholar 

  30. Adkins R.M., Gelke E.L., Rowe D., Honeycutt R.L. 2001. Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol. Biol. Evol., 18, 777–791.

    PubMed  CAS  Google Scholar 

  31. Steppan S.J., Adkins R.M., Anderson J. 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst. Biol. 53, 533–553.

    Article  PubMed  Google Scholar 

  32. Farris J.S., Kallersjo M., Kluge A.G., Bult C. 1995. Constructing a significance test for incongruence. Syst. Biol. 44, 570–572.

    Google Scholar 

  33. Posada D., Crandall K.A. 1998. Modeltest: Testing the model of DNA substitution. Bioinformatics. 14, 817–818.

    Article  PubMed  CAS  Google Scholar 

  34. Thorne J.L., Kishino H. 2002. Divergence time and evolutionary rate estimation with multilocus data. Syst. Biol. 51, 689–702.

    Article  PubMed  Google Scholar 

  35. Steppan S.J., Adkins R.M., Spinks P.Q., Hale C. 2005. Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Mol. Phylogen. Evol. 37, 370–388.

    Article  CAS  Google Scholar 

  36. Barker F.K., Lutzoni F.M. 2002. The utility of the incongruence length difference test. Syst. Biol. 51, 625–637.

    Article  PubMed  Google Scholar 

  37. Lebedev V.S., Ivanova N.V., Pavlova, N.K., Poltoraus A.B., 2003. Molecular phylogeny of Palearctic hamsters. In: Sistematika, filogeniya i paleontologiya melkikh mlekopitayushchikh (Systematics, Phylogeny, and Paleontology of Small Mammals). Eds. Averyanov A.O., Abramson N.I. St. Petersburg: Zool. Inst. Ross. Akad. Nauk, pp. 114–118.

    Google Scholar 

  38. Robovsky J., Ricankova V., Zrzavy J. 2008. Phylogeny of arvicolinae (Mammalia, Cricetidae): utility of morphological and molecular data sets in a recently radiating clade. Zool. Scr. 37, 571–590.

    Article  Google Scholar 

  39. Waddell P. J., Cao Y. Hauf J., Hasegawa M. 1999. Using novel methods to evaluate mammalian mtDNA and detect internal conflicts: including AA invariant sites-Log-Det and site stripping, with special reference to the position of hedgehog, armadillo, and elephant. Syst. Biol. 48, 31–53.

    Article  PubMed  CAS  Google Scholar 

  40. Lin Y.-H., McLenachan P.A., Gore A.R, Phillips M.J., Ota R., Hendy M.D., Penny D., 2002. Four new mitochondrial genomes and the increased stability of evolutionary trees of mammals from improved taxon sampling. Mol. Biol. Evol. 19, 2060–2070.

    PubMed  CAS  Google Scholar 

  41. Agajanyan A.K. 1992. New volelike rodents (Mammalia, Rodentia) from the Russian Plain Pliocene. Paleontol. Zh. 2, 99–111.

    Google Scholar 

  42. Gromov I.M., Erbaeva M.A. 1995. Mlekopitayushchie fauny Rossii i sopredel’nykh territorii (Zaitseobraznye i gryzuny) (Mammals in the Fauna of Russia and Neighboring Countries: Lagomorphs and Rodents). St Petersburg: Nauka.

    Google Scholar 

  43. Pavlinov I.Ya. 2003. Sistematika sovremennykh mlekopitayushchikh (The System of Recent Mammals). Moscow: Mosk. Gos. Univ.

    Google Scholar 

  44. Zubtsova G.E. 1978. Morphological features of incisor structure in Burrowing rodents as related to the type of burrowing: 1. Mole rats (Spalax), mole voles (Ellobius), and five-toed jerboas (Allactaginae). In: Funktsional’naya morfologiya i sistematika mlekopitayushchikh (Functional Morphology and Taxonomy of Mammals). Leningrad: Zool. Inst. Akad. Nauk SSSR, pp. 105–108.

    Google Scholar 

  45. Zheng S.H., Zhang Z.Q., Cui N. 2004. On some species of Prosiphneus (Siphneidae, Rodentia) and the origin of Siphneidae. Vertebrata PalAsiatica, 42, 297–315.

    Google Scholar 

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Authors and Affiliations

  1. Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034, Russia

    N. I. Abramson

  2. Zoological Museum, Moscow State University, Moscow, 125009, Russia

    V. S. Lebedev

  3. Geological Institute, Russian Academy of Sciences, Moscow, 119017, Russia

    A. S. Tesakov

  4. Biology Department, Moscow State University, Moscow, 119991, Russia

    A. A. Bannikova

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  1. N. I. Abramson
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  2. V. S. Lebedev
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  3. A. S. Tesakov
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  4. A. A. Bannikova
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Correspondence to N. I. Abramson.

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Original Russian Text © N.I. Abramson, V.S. Lebedev, A.S. Tesakov, A.A. Bannikova, 2009, published in Molekulyarnaya Biologiya, 2009, Vol. 43, No. 5, pp. 897–909.

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Abramson, N.I., Lebedev, V.S., Tesakov, A.S. et al. Supraspecies relationships in the subfamily Arvicolinae (Rodentia, Cricetidae): An unexpected result of nuclear gene analysis. Mol Biol 43, 834–846 (2009). https://doi.org/10.1134/S0026893309050148

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  • DOI: https://doi.org/10.1134/S0026893309050148

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