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Ther9 2 071 081 Lissovsky.P65 Russian J. Theriol. 9(2): 7181 © RUSSIAN JOURNAL OF THERIOLOGY, 2010 Geographic variation of Microtus middendorffii (Cricetidae, Arvicolinae, Rodentia) sensu lato studied by craniometrical and mitochondrial features Andrey A. Lissovsky, Ekaterina V. Obolenskaya, Natalia I. Abramson, Nikolai E. Dokuchaev, Valeriy V. Yakimenko, Marina G. Malkova, Alexey S. Bogdanov & Natalia V. Ivanova ABSTRACT. Morphometric variation of voles Microtus middendorffii sensu lato and M. gromovi was examined based on 221 skulls. Molecular variation was assessed on partial sequences of cytochrome C oxidase subunit I gene (657 bp) from 23 individuals of M. middendorffii s.l. The observed pattern of variation within M. middendorffii s.l. corresponds to polytypic species comprising a number of geographic races. The taxonomic rank of the Ural and Yamal race (M. m. ryphaeus) is not lower than the rank of M. m. middendorffii and M. m. hyperboreus. Essential morphological differences within the scope of this study were found for the sample from the Kochechum River. The voles of M. gromovi are very similar morphologically to M. middendorffii. Taxa M. middendorffii, M. gromovi, and M. mongolicus form the single clade on the mitochondrial based tree, with M. gromovi as a basal taxon. KEY WORDS: Microtus middendorffii, Microtus hyperboreus, Microtus gromovi, geographic variation. Andrey A. Lissovsky [[email protected]] and Ekaterina V. Obolenskaya [[email protected]], Zoolog- ical Museum of Moscow State University, Bolshaya Nikitskaya 6, Moscow 125009, Russia; Natalia I. Abramson [[email protected]], Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, Saint Petersburg 199034, Russia; Nikolai E. Dokuchaev [[email protected]], Institute of Biological Problems of the North, Far East Branch of the Russian Academy of Sciences, ul. Portovaya 18, Magadan 685000, Russia; Valeriy V. Yakimenko [[email protected]] and Marina G. Malkova, Omsk scientific-research institute of naturel-foci infections, Mira prospekt 7, Omsk 644080, Russia; Alexey S. Bogdanov [[email protected]], Koltzov Institute of Developmental Biology, Vavilova 26, Moscow 119991, Russia; Natalia V. Ivanova [[email protected]], Biodiversity Institute of Ontario, University of Guelph, Guelph, Ontario, Canada N1G 2W1. Ãåîãðàôè÷åñêàÿ èçìåí÷èâîñòü êðàíèîìåòðè÷åñêèõ è ìèòîõîíäðèàëüíûõ ïðèçíàêîâ Microtus middendorffii (Cricetidae, Arvicolinae, Rodentia) sensu lato À.À. Ëèñîâñêèé, Å.Â. Îáîëåíñêàÿ, Í.È. Àáðàìñîí, Í.Å. Äîêó÷àåâ, Â.Â. ßêèìåíêî, Ì.Ã. Ìàëüêîâà, À.Ñ. Áîãäàíîâ, Í.Â. Èâàíîâà ÐÅÇÞÌÅ. Èññëåäîâàíà âûáîðêà èç 221 ÷åðåïà ïðåäñòàâèòåëåé Microtus middendorffii sensu lato è M. gromovi. Ãåíåòè÷åñêèå äàííûå ïî ó÷àñòêó ãåíà öèòîõðîì Ö îêñèäàçû (657 ïàð îñíîâàíèé) ïîëó÷åíû îò 23 ýêçåìïëÿðîâ M. middendorffii s.l. Íàáëþäàåìàÿ êàðòèíà èçìåí÷èâîñòè âíóòðè M. middendorffii s.l. áîëåå âñåãî ñîîòâåòñòâóåò ïîëèòèïè÷åñêîìó âèäó, ïðåäñòàâëåííîìó íåñêîëüêèìè ãåîãðàôè÷åñ- êèìè ôîðìàìè. Ðàíã óðàëî-ÿìàëüñêîé ôîðìû (M. m. ryphaeus) íå íèæå, ÷åì M. m. middendorffii è M. m. hyperboreus. Ñóùåñòâåííûå, â ìàñøòàáå èññëåäîâàíèÿ, ìîðôîëîãè÷åñêèå îòëè÷èÿ õàðàêòåðèçó- þò âûáîðêó ñ ð. Êî÷å÷óì. Ìîðôîëîãè÷åñêè ïðåäñòàâèòåëè M. gromovi î÷åíü áëèçêè ê M. middendorffii. Òàêñîíû M. middendorffii, M. gromovi è M. mongolicus îáðàçóþò åäèíóþ êëàäó íà ìèòîõîíäðèàëü- íîì äåðåâå, áàçàëüíîå ïîëîæåíèå â ýòîé êëàäå çàíèìàåò M. gromovi. ÊËÞ×ÅÂÛÅ ÑËÎÂÀ: Microtus middendorffii, Microtus hyperboreus, Microtus gromovi, ãåîãðàôè÷åñ- êàÿ èçìåí÷èâîñòü. 72 A.A. Lissovsky, E.V. Obolenskaya, N.I. Abramson et al. Introduction The sample contained 221 intact skulls of M. midden- dorffii s.l. and M. gromovi (Appendix I). Debates on the taxonomic status of the Middendor- Fifteen measurements were taken with electronic ffs vole (Microtus middendorffii Poljakov, 1881) and caliper (with an accuracy of 0.01 mm) from each skull the north Siberian vole (M. hyperboreus Vinogradov, as follows: condylobasal length, minimal distance be- 1933) have a long history. It was reviewed in detail tween maxillary toothrows, diastemal length, alveolar earlier (Meyer et al., 1996; Litvinov, 2001; Volpert & length of maxillary toothrow, zygomatic breadth, max- Shadrina, 2002). The study comparing all previous imal width between lateral edges of auditory bullae, opinions is, however, still absent. This makes the dis- skull height at the level of maxillary toothrows, orbital cussed concepts ambiguous and unreliable. length and width, width of rostrum base, orbital con- The discussion always focused on the species or striction, length of auditory bulla, width of auditory subspecies rank of M. hyperboreus. The other taxa, bulla, alveolar length of mandibular toothrow, distance mentioned from time to time, were classified a priori between the base of incisor and the apex of mandibular either to M. m. middendorffii, or to M. m. hyper- articular process. All calculations were performed based boreus. on logarithmic measurements. Morphological characters differentiating M. m. mid- We used the skulls of voles of different ages. All dendorffii and M. m. hyperboreus are described in a skulls were divided into three age categories (Liss- number of publications (Vinogradov, 1933; Ognev, ovsky & Obolenskaya, 2010) corresponded to obvious- 1950; Vinogradov & Gromov, 1952; Krivosheev, 1971; ly juvenile (1), obviously adult with developed crests Pokrovskiy et al., 1975; Gromov & Polyakov, 1977; on the skull (3), and all others (2). Meyer et al., 1996; Litvinov, 2001). Following these We used hierarchical two-factor MANOVA with descriptions, different authors separated M. m. midden- geographical sample and sex treated as factors (sex dorffii from M. m. hyperboreus in collections. But it is nested in sample), in order to evaluate significance of impossible to find two publications where the composi- differences between sexes. For this purpose we studied tion of taxa distinguished on the base of the same five samples of individuals from age group 2 with characters would coincide (Ognev, 1950; Krivosheev, approximately equal ratio of males and females. 1971; Gromov & Polyakov, 1977; Meyer et al., 1996; In order to exclude age bias from morphometric Litvinov, 2001; Volpert & Shadrina, 2002). In other analysis, we used an orthogonal projection of initial words, different authors starting from the same points data along the vector of age variation (Burnaby, 1966). referred the same specimens to different taxa. There- The vector of age variation was calculated as the first fore, the morphological variation of M. middendorffii eigenvector of the between-group covariance matrix. sensu lato needs quantitative evaluation. We used only the first and the third age classes during Another issue, which has not been addressed yet, is calculations of the covariance matrix in order to avoid the morphological distinctiveness of M. gromovi an error induced by inaccuracy in determining the sec- Vorontsov et al., 1988. As inferred from the data on ond age class. There were seven samples included in cytochrome b gene (Bannikova et al., 2010) and the this analysis. general habitus of this vole, it is very close to M. The samples for hierarchical cluster analysis in- middendorffii. It is, therefore, important to evaluate the cluded only specimens collected in the same locality morphological similarity between these two species (44 samples total). Only samples with n>3 were used in and estimate the probability of their morphological cluster analysis (20 samples). Cluster analysis was per- misidentification. formed on the basis of a matrix of Mahalanobis distanc- Thus, the main task of the present study is to give a es using the unweighted pair group method with arith- quantitative estimation of variation in M. middendorffii metic mean (UPGMA). The bias induced by using s.l. and M. gromovi. We intentionally avoid discussing samples of different sizes was corrected (Marcus, 1993). the nomenclatorial questions here and will use the es- An analysis of posterior probabilities was performed tablished names. using canonical discriminant analysis. The learning sam- ple was composed of specimens used in cluster analysis Materials and methods and divided into groups according to its result. The ordination was performed using the axes of canonical space calculated with grouping variable con- Specimens used in the morphometric study were taining geographical samples with n>3. taken from the collections of the Zoological Museum of Craniometric data were processed using standard Moscow State University (ZMMU), Zoological Insti- modules of STATISTICA 8.0 (StatSoft 2007) and sev- tute of the Russian Academy of Science, St-Petersburg eral custom algorithms written by the first author using (ZIN), Institute of Systematics and Ecology of Ani- Statistica Visual Basic programming language. mals, Siberian Branch of the Russian Academy of Sci- A fragment of mitochondrial gene cytochrome oxi- ence (ISEA), Institute of Plant and Animal Ecology, dase subunit 1 (COI) 657bp in length from 23 speci- Ural Branch of the Russian Academy of Science (IPAE), mens of M. middendorffii s.l. from 8 geographical lo- Institute of Biological Problems of North, Far East calities (Appendix II) was used for the study of genetic Branch of the Russian Academy of Science (IBPN). Geographic variation of Middendorffs vole 73 Figure 1. The dendrogram showing results of hierarchical cluster analysis of craniometric features of Microtus middendorffii s.l. and M. gromovi samples. For explanations of sample labels, refer to Appendix I. differentiation.
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