Analysis of shape and size variation of the first lower molar in Far-Eastern grey voles of genus Alexandromys (Rodentia: Cricetidae) from Russian fauna using geometric morphometrics

Analysis of shape and size variation of the first lower molar in Far-Eastern grey voles of genus Alexandromys (Rodentia: Cricetidae) from Russian fauna using geometric morphometrics

Voyta L.L., Golenishchev F.N., Tiunov M.P.

P. 19-32

The variation of quantitative characters of the first lower molar was analysed in nine species of Far-Eastern voles Alexandromys from Russian fauna. Canonical variation analysis revealed that main differences were associated with “oeconomus-like” fusion, and clearly differentiates A. oeconomus, A. mongolicus and A. gromovi from other species. The results of UPGMA cluster analysis based on the average Procrustes distances did not agree with recent molecular studies. Discriminant analysis of Procrustes coordinates of 19 landmarks showed that the percentage of correct species classifications of samples vary from 50% to 100%. Linear measurements together with shape features can be used for identification of the following species: A. oeconomus, A. mongolicus, and A.sachalinensis. Shape of enamel loops of the first lower molar of Far-Eastern grey voles can be used for species identification, but not for phylogenetic analysis.DOI: 10.15298/rusjtheriol.12.1.02

Literature
  • Abramson N.I. & Lissovsky A.A. 2012. Subfamily Arvicolinae Gray 1821 // Pavlinov I.Ya. & Lissovsky A.A. (eds.). The Mammals of Russia: A Taxonomic and Geographic Reference. (Archives of Zoological Museum of MSU. Vol.52. Moscow: KMK Sci Press. P.220-276.
  • Agadzhanian A.K. & Yatsenko V.N. 1984. [Phylogenetic relationships of North Eurasian voles] // Rossolimo O.L. (ed.). [Problems of variation and phylogeny of mammals]. Moskva: Izdatel'stvo Moskovskogo Gosudarstvennogo Universiteta. P.135-190 [in Russian].
  • Angermann R. 1973. [Homologous variation of molars in voles (Microtinae)] // Vorontsov N.N. (ed.). [Problems of Evolution]. Vol.3. Novosibirsk: Izdatel'stvo Nauka. P.104-118 [in Russian, with English summary].
  • Bannikova A.A., Lebedev V.S., Lissovsky A.A., Matrosova V., Abramson N.I., Obolenskaya E.V. & Tesakov A.S. 2010. Molecular phylogeny and evolution of the Asian lineage of vole genus Microtus (Rodentia: Arvicolinae) inferred from mitochondrial cytochrome b sequence // Biological Journal of the Linnean Society. Vol.99. P.595-613.
  • Baryshnikov G.F. & Puzachenko A.Yu. 2009. Craniometrical variability in insular populations of brown bear (Ursus arctos, Carnivora) from Hokkaido, Sakhalin and South Kurils // Proceedings of the Zoological Institute RAS. Vol.313. No.2. P.119-142.
  • Bookstein F.L. 1991. Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge: Cambridge University Press. 435 p.
  • Butler P.M. 1985. Homologies of molar cusps and crests, and their bearing on assessment of rodent phylogeny // Luckett W.P. & Hartenberger J.-L. (eds.). Evolutionary Relationships among Rodents: A Multidisciplinary Analysis. New York: Plenum Press. P.381-401.
  • Caumul R. & Polly P.D. 2005. Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota, Rodentia) // Evolution. Vol.59. P.2460-2472.
  • Courant F., Brunet-Lecomte P., Volobuev V., Chaline J., Quere J.P., Nadachowski A., Mountire S., Bao G., Viriot L., Rausch R., Erbajeva M., Shi D. & Girauduox P. 1999. Karyological and dental identification of Microtus limnophilus in a large focus of alveolar echinococcosis (Gansu, China) // Comptes Rendus de L'Académie des Sciences. Série 3. Sciences de la Vie. Vol.322. P.473-480.
  • Frisman L.V., Korobitsyna K.V., Kartavtseva I.V., Sheremetyeva I.N. & Voyta L.L. 2009. Voles (Microtus Schrank, 1798) of the Russian Far East: allozymic and karyological divergence // Russian Journal of Genetics. Vol.45. No.6. P.707-714.
  • Gileva E.A. 1972. [Chromosomal polymorphism in two related taxa of subarctic voles (North Siberian vole and Middendorff's vole)] // Doklady Akademii Nauk SSSR. Vol.203. No.3. P.689-692 [in Russian].
  • Golenishchev F.N. 1982. [Grey voles (subgenus Microtus, species-group maximowiczii) of East Siberia and Far East]. PhD Thesis. Leningrad: Zoologicheskii Institut AN SSSR. 23 p. [in Russian].
  • Gromov I.M. & Erbajeva M.A. 1995. [The Mammals of Russia and Adjacent Territories. Lagomorphs and Rodents]. Sankt-Peterburg: Izdatel'stvo Zoologicheskogo Instituta. 520 p. [in Russian].
  • Gromov I.M., Gureev A.A., Novikov G.A., Sokolov I.I., Strelkov P.P. & Chaptsky K.K. 1963. [Mammals of Fauna of USSR. Part1.]. Moskva-Leningrad: Izdatelstvo Akademii Nauk SSSR. 638 p. [in Russian].
  • Gromov I.M. & Polyakov I.Ya. 1977. [Fauna of the USSR, Voles (Microtinae): Mammals]. Leningrad: Izdatel'stvo Nauka. Vol.3. No.8. 504 p. [in Russian].
  • Hammer Ш, Harper D.A.T. & Ryan P.D. 2001. Paleontological Statistics Software Package for Education and Data Analysis // Palaeontologia Electronica. Vol.4. P.1-9.
  • Haring E., Sheremetyeva I.N. & Kryukov A.P. 2011. Phylogeny of Palearctic vole species (genus Microtus, Rodentia) based on mitochondrial sequences // Mammalian Biology. Vol.76. P. 258-267.
  • Hinton M.A.C. 1929. Monograph of the Voles and Lemmings (Microtinae) Living and Extinct. London: British Museum (Natural History). Vol.1. 488 p.
  • Kartavtseva I.V., Sheremetyeva I.N., Korobitsina K.V., Nemkova G.A., Konovalova E.V., Korablev V.V. & Voyta L.L. 2008. Chromosomal forms of Microtus maximowiczii (Schrenck, 1859) (Rodentia, Cricetidae): variation in 2n and NF in different geographic regions // Russian Journal of Theriology. Vol.7. No.2. P.89-97.
  • Kazantseva N.E. & Tesakov A.S. 1998. Evolution of Plio-Pleistocene voles with the special reference to demographic features of fossil assemblages // Mededelingen Nederlands Instituut voor Toegepaste Geowetenschappen TNO. Vol.60. P.555-564.
  • Klingenberg C.P. 2011. MorphoJ: an integrated software package for geometric morphometrics // Molecular Ecology Resources. Vol.11. P.353-357.
  • Koenigswald W. 1980. Schmelzstruktur und Morphologie in den Molaren der Arvicolidae (Rodentia) // Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft. Bd.539. 129 p.
  • Kotlia B.S. & Mathur D.P. 1992. Morphologic, sinumetric and enamel investigation of the Pliocene arvicolids (Rodentia) from the Karewas of the Kashmir, India // Geobios. Vol.25. No.6. P.781-796.
  • Kovalskaja Yu.M., Khotolhu N. & Orlov V.N. 1980. [Geographical distribution of chromosomal mutations and intraspecific structure of Microtus maximowiczii (Rodentia, Cricetidae)] // Zoologicheskii Zhurnal. Vol.59. No.12. P.1862-1869 [in Russian].
  • Kuziakin A.P. 1963. [To the systematics of Rodents of fauna of USSR] // Trudy Moskovskogo Obshestva Ispytatelei Prirody. Vol.10. P.105-115 [in Russian].
  • Larina N.I. 1974. [To the method of age determination in rootless voles group] // Shlyakhtin G.V. (ed.). [Physiological and Population Ecology of Animals]. Vol.2. No.4. Saratov: Izdatel'stvo Saratovskogo Universiteta. P.92-97 [in Russian].
  • Lissovsky A.A., Obolenskaya E.V., Abramson N.I., Dokuchaev N.E., Yakimenko V.V., Mal'kova M.G., Bogdanov A.S. & Ivanova N.V. 2010. Geographic variation of Microtus middendorffii (Cricetidae, Arvicolinae, Rodentia) sensu lato studied by craniometrical and mitochondrial features // Russian Journal of Theriology. Vol.9. No.2. P.71-81.
  • Lissovsky A.A. & Obolenskaya E.V. 2010. [Structure of craniometric variation of root vole (Microtus oeconomus, Rodentia)] // Zoologicheskii Zhurnal. Vol.89. No.6. P.1-5 [in Russian, with English summary].
  • Lissovsky A.A. & Obolenskaya E.V. 2011. [The structure of craniometrical diversity of grey voles Microtus subgenus Alexandromys] // Proceedings of Zoological Institute RAS. Vol.315. No.4. P.461-477 [in Russian, with English summary].
  • Litvinov Yu.N. 2001. [Communities and Populations of Small Mammals in Siberian Ecosystems]. Novosibirsk: Izdatel'stvo TSERIS. 128 p. [in Russian].
  • Martin R.A. 1998. Time's arrow and the evolutionary position of Orthriomys and Herpethomys // Paludicola. Vol.2. No.1. P.70-73.
  • McGuire J.L. 2010. Geometric morphometrics of vole (Microtus californicus) dentition as a new paleoclimate proxy: shape change along geographic and climatic clines // Quaternary International. Vol.212. P.198-205.
  • McGuire J.L. 2011. Identifying California Microtus species using geometric morphometrics documents Quarternary geographic range contractions // Journal of Mammalogy. Vol.92. No.6. P.1383-1394.
  • Meyer M.N., Golenishchev F.N., Radjably S.I. & Sablina O.V. 1996. [Voles (Subgenus Microtus Schrank) of Russia and Adjacent Territories]. (Proceedings of the Zoological Institute. Vol.232.). Sankt-Peterburg: Izdatel'stvo Rossiiskoi Akademii Nauk. 320 p. [in Russian].
  • Ognev S.I. 1950. [The Mammals of the USSR and Adjacent Territories. Rodents]. Vol.7. Moskva-Leningrad: Izdatel'stvo AN SSSR. 706 p. [in Russian].
  • Orlov V.N., Shvetsov Yu.G., Kovalskaya Yu.M., Kutashova T.S. & Stupina A.G. 1974. [Diagnosis and distribution of voles Microtus maximowiczii and M. fortis (Rodentia, Cricetidae) within Transbaikalia] // Zoologicheskii Zhurnal. Vol.53. No.9. P.1391-1396 [in Russian].
  • Polly P.D. 2007. Phylogeographic differentiation in Sorex araneus: morphology in relation to geography and karyotype // Russian Journal of Theriology. Vol.6. P.73-84.
  • Poljakov I.S. 1881. [Taxonomical review of Siberian voles] // Zapiski Imperatorskoy Akademii Nauk. Vol.39. Suppl.2. P.1-91 [in Russian].
  • Pozdniakov A.A. 1993. [Morphotypical variation of molar teeth occlusal surface of the grey voles of species-group maximowiczii (Rodentia, Cricetidae): an experience of quantitative statistic analysis] // Zoologicheskii Zhurnal. Vol.72. No.11. P.114-125 [in Russian].
  • Rabeder G. 1981. Die Arvicoliden (Rodentia, Mammalia) aus dem Pliozan und dem alteren Pleistozan von Niederosterreich // Beitrage der Palaontologisch Osterreich. Bd.8. S.1-373.
  • Rohlf F.G. & Slice D.E. 1990. Extension of the Procrustes method for the optimal superimposition of landmarks // Systematic Zoology. Vol.39. P.40-59.
  • Rörig G. & Börner C. 1905. Studien über das Gebiss mitteleuropäischer rezenter Mäuse // Arbeiten aus der Kaiserlichen Biologischen Anstalt für Land- und Forstwirtschaft. Bd.5. No.2. P.37-89.
  • Sheets H.D. 2001. IMP Software Series. Buffalo, New York, Canisius College.
  • Sheremetyeva I.N., Kartavtseva I.V., Voyta L.L., Kryukov A.P. & Haring E. 2009. Morphometric analysis of intraspecific variation in Microtus maximowiczii (Rodentia, Cricetidae) in relation to chromosomal differentiation with reinstatement of Microtus gromovi Vorontsov et al., 1988, stat. nov. // Journal of Zoological Systematics and Evolutionary Research. Vol.47. P.42-48.
  • Sheremetyeva I.N., Kartavtseva I.V., Voyta L.L. & Tiunov M.P. 2010. [New data on distribution of voles of the genus Microtus (Rodentia, Cricetidae) from the Russian Far East] // Zoologicheskii Zhurnal. Vol.89. No.10. P.1273-1276 [in Russian, with English summary].
  • 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 Publ. 336 p.
  • Tesakov A.S. 2005. Pliocene voles (Pliomys, Arvicolinae, Radentia) from Odessa Catacombs // Russian Journal of Theriology. Vol.4. No.2. P.123-135.
  • Tiunov I.M., Tiunov M.P. & Sheremetyeva I.N. 2009. [Findings of Mongolian toad (Bufo raddei) and reed vole (Microtus fortis) on Sakhalin Island] // Zoologicheskii Zhurnal. Vol.88. No.11. P.1406-1408 [in Russian, with English summary].
  • Van der Meulen A.J. 1973. Middle Pleistocene smaller mammals from the Monte Peglia (Orivieto, Italy) with special reference to the phylogeny of Microtus (Arvicolidae, Rodentia) // Quaternaria. Vol.17. P.1-144.
  • Vinogradov B.S. 1933. [Mammals of USSR. Rodents]. Leningrad: Izdatel'stvo AN SSSR. 87 p. [in Russian].
  • Vinogradov B.S. & Gromov I.M. 1952. [The Rodents of Fauna of USSR]. Leningrad: Izdatel'stvo AN SSSR. 298 p. [in Russian].
  • Vorontsov N.N., Boeskorov G.G., Lyapunova E.A. & Revin Yu.V. 1988. [A new chromosome form and variation in Microtus maximowiczii (Rodentia, Cricetidae)] // Zoologicheskii Zhurnal. Vol.67. No.2. P.205-213 [in Russian, with English summary].
  • Voyta L.L. & Golenishchev F.N. 2007. [Geometric morphometrics of molars in three species of the common field voles, the subgenus Alexandromys (Rodentia: Cricetidae: Microtus)] // Rozhnov V.V. & Tembotova F.A. (eds.). [Mammals of Mountain Territories]. Moskva: KMK Scientific Press. P.79-84 [in Russian].
  • Voyta L.L. & Golenishchev F.N. 2008. Analysis of variation of the molars in grey voles Microtus Schrank, 1798 (Rodentia: Cricetidae: Arvicolinae) using methods of geometric morphometrics // Abstracts of the 11-th International Conference on Rodent Biology. Rodents et Spatium. Myshkin, Russia, 24-28 July 2008. Moscow: KMK Sci Press. P.149-150.
  • Voyta L.L., Golenishchev F.N., Tiunov M.P. & Panasenko V.E. 2011. Some restrictions of the morphometric methods as applied to classification of fossil remains of Sorex (Eulipotyphla: Soricidae) and Microtus (Rodentia: Cricetidae) // Abstracts of the 6-th European Congress of Mammalogy. Paris, France, 19-23 July 2011. Paris: Université Pierre et Marie Curie. P.39.
  • Zagorodnyuk I.V. 1990. [Karyotypic variation and systematics of the grey voles (Rodentia, Arvicolini). Communication 1. Species composition and chromosomal numbers] // Vestnik Zoologii. Vol.2. P.26-37 [in Russian].
  • Zelditch M.L., Swiderski D.L., Sheets H.D. & Fink W.L. 2004. Geometric Morphometrics for Biologists: A Primer. San Diego: Elsevier Academic Press. 437 p.
  • Zimmermann K. 1952. Die Simplex-Zahnform der Feldmaus Microtus arvalis Pallas // Verhandlung der Deutschen Zoologischen Gesellschaft. Bd.46. P.492-498.
  • Zimmermann K. 1959. Uber eine Kreuzung von Unterarten der Feldmaus // Zoologische Jahrbucher. Bd.87. No.1-2. P.1-12.