Abstract
The East European vole is a facultative synanthropic species that actively spreads in the eastern part of northern Eurasia. The distribution area of the species in Irkutsk oblast has been known as a disjunct part of the range since the 1980s. Our dataset includes 98 individuals caught in 2016–2017 and 2021–2023 in the eastern segment of the species’dispersal area, where the East European vole was first discovered in the early 2010s. Animals were caught in anthropogenically transformed landscapes spanning from the outskirts of Irkutsk to kilometer 23 of the Goloustnenskii Tract; trapping in natural biotopes revealed no M. rossiaemeridionalis. Species identification was based on molecular genetic markers. Morphological and fine structural characteristics of molar teeth were studied using both light and scanning electron microscopy. The complexity of the occlusal surface, the alternation patterns of the enamel cutting edges (occlusal regularity), and the presence or absence of atypical extra elements such as prismatic folds and prisms in places of the early cricetid dental features were assessed. The estimates of the complexity and regularity patterns fell within the range of dental variability known for the continuous distribution area of the species. The atypical extra elements on molars were described in M. rossiaemeridionalis for the first time based on material coming from two trapping sites. With the maximum manifestation of these folds, a supernumerary prism, topologically corresponding to the hypoconid, is separated from the posterior lobe of the lower teeth. The distribution of lamellar and radial enamel on the supernumerary prism is not consistent with the functionally significant and evolutionarily determined distribution of enamel types on teeth of the genus Microtus. It is concluded that the studied local micropopulation exhibits the phenotypic consequences of population restoration from a small number of founders. Apparently, the species in the study area faces multiple successive cases of establishment (naturalization) in a new territory. The results obtained confirm the prospects of using dental characters for monitoring Arvicolinae species, the distribution boundaries of which are subject to significant spatial changes in the relatively short periods of time available for observation.
REFERENCES
Allendorf, F.W. and Lundquist, L.L., Introduction: population biology, evolution, and control of invasive species, Conserv. Biol., 2003, vol. 17, pp. 24–30.
Bayanova, A.A., Analysis of the fire rate of forest resources in the Irkutsk oblast, Monitoring. Nauka Tekhnol., 2018, no. 2, pp. 35–38.
Blackburn, T.M., Pyšek, P., Bacher, S., Carlton, J.T., Duncan, R.P., Jarošık, V., Wilson, J.R.U., and Richardson, D.M., A proposed unified framework for biological invasions, Trends Ecol. Evol., 2011, vol. 26, pp. 333–339.
Broad Institute, Microtus ochrogaster genome assembly M-icOch1.0, 2012. www.ncbi.nlm.nih.gov/assembly/GCF_ 000317375.1. Updated December 7, 2012. Accessed April 25, 2023.
Chaline, J., Les rongeurs du Pleistocene moyen et superieur de France (Systematique–Biostratigraphie–Paleoclimatologie), Cah. Paleontol., Paris: C.N.R, 1972.
Chapelle, V. and Silvestre, F., Population epigenetics: the extent of DNA methylation variation in wild animal populations, Epigenomes, 2022, vol. 6, no. 4, p. 31.
Cheprakov, M.I., Phenotypic variation and inheritance of an atypical form of the M1 anterior lobe of collared lemmings (Dicrostonyx, Rodentia, Arvicolinae), Biol. Bull. (Moscow), 2022, vol. 49, no. 5, pp. 438–443.
Cho, S.-W., Kwak, S., Woolley, T.E., Lee, M.J., Kim, E.J., Baker, R.E., Kim, H.J., Shin, J.S., Tickle, C., Maini, P.K., and Jung, H.S., Interactions between Shh, Sostdc1 and Wnt signalling and a new feedback loop for spatial patterning of the teeth, Development, 2011, vol. 138, pp. 1807–1816.
Demidovich, A.P., Anthropogenic transformation of rodent communities as a component of parasitic systems, Byull. VSNTs SO RAMN, 2006, no. 2 (48), pp. 28–33.
Demidovich, A.P., Rodent communities of agricultural lands of the Irkutsk oblast, Vestn. Irkutsk. Gos. S-kh. Akad., 2016, no. 76, pp. 97–102.
Galiana, N., Lurgi, M., Montoya, J.M., and Lopez, B.C., Invasions cause biodiversity loss and community simplification in vertebrate food webs, Oikos, 2014, vol. 123, no. 6, pp. 721–728.
Genome Reference Consortium, Mouse Build 39 (GRCm39), 2020. https://www.ncbi.nlm.nih.gov/assembly/GCF_000001635.27. Updated June 24, 2020. Accessed April 25, 2023.
Genome Reference Consortium, Human Build 38 patch release 14 (GRCh38.p14), 2022. https://www.ncbi.nlm.nih.gov/assembly/GCF_000001405.40. Updated February 3, 2022. Accessed April 25, 2023.
Gileva, E.A., The b chromosome system in the varying lemming Dicrostonyx torquatus Pall., 1779 from natural and laboratory populations, Russ. J. Genet., 2004, vol. 40, pp. 1399–1406.
Gileva, E.A. and Chebotar, N.A., Fertile XO males and females in the varying lemming, Dicrostonyx torquatus Pall. (1779), Heredity, 1979, vol. 42, pp. 67–77.
Janossy, D. and Schmidt, E., Extreme Varianten des M1 der Feldmaus (Microtus arvalis Pallas) in Ungarn, Vertebr. Hung., 1960, vol. 2, pp. 137–142.
Janossy, D. and Schmidt, E., Extreme Varianten des M1 der Feldmaus (Microtus arvalis Pallas) in Ungarn. II, Z. Säugetierkunde, 1975, vol. 40, pp. 34–36.
Jentzsch, M., Kraft, R., Lemkul, A., Kapischke, H.-J., Maternowski, H.J., and Wolf, R., Anomalies and pathological changes of skulls and dentition of wild small mammal species from Germany, J. Vertebr. Biol., 2020, vol. 69, no. 4, p. 20072.
Kangas, A.T., Evans, A.R., Thesleff, I., and Jernvall, J., Nonindependence of mammalian dental characters, Nature, 2004, vol. 432, pp. 211–214.
Kapischke, H., Zur Variabilität der Zähne von Feldmäusen Microtus arvalis (Pallas, 1779) aus Sachsen (Übersicht zu einer Sammlung im Rahmen des Projektes: Atlas der Säugetiere Sachsens), Veroffentlichungen des Museums der Westlausitz Kamenz, 2014, no. 32, pp. 85–110.
Kapischke, H., Wilhelm, M., and Fabian, K., Zahnbesonderheit einer Feldmaus Microtus arvalis aus E-ulengewöllen, Ornithol. Mitteilungen, 2015, no. 67, p. 128.
von Koenigswald, W., Schmeltzstruktur und Morphologie in den Molaren der Arvicolidae (Rodentia), Abhandlungen der Senckenbergische Naturforschende Gesellschaft, 1980, vol. 239, pp. 1–139.
Korablev, N.P., Korablev, P.N., and Korablev, M.P., Mikroevolyutsionnye protsessy v populyatsiyakh translotsirovannykh vidov: evroaziatskii bobr, enotovidnaya sobaka, amerikanskaya norka (Microevolutionary Processes in Populations of Translocated Species: Eurasian Beaver, Raccoon Dog, and American Mink), Moscow: KMK, 2018.
Kovalenko, E.E., The effect of trait norm and its theoretical significance, in Evolyutsionnaya biologiya: istoriya i teoriya (Evolutionary Biology: History and Theory), Kolchinskii, E.I. and Popov, I.Yu., Eds.-in-Chief, St. Petersburg: Politekhnika-Servis, 2003, pp. 66–87.
Kraft, R., Ungewöhnliche Molarenbildungen bei Feldmaus (Microtus arvalis) und Erdmaus (Microtus agrestis), Säugetierkundliche Informationen, 2000, nos. 23–24, pp. 587–589.
Lipin, S.I., Khromichek, S.I., Pokhryaeva, A.N., Sukhanov, N.A., Mironchuk, Yu.V., and Yakubenok, M.I., The East European vole is a carrier of tularemia in the southern regions of Eastern Siberia, in Voprosy regional’noi gigieny, sanitarii i epidemiologii, Nauchno-prakt. konf., Tezisy dokladov (Issues of Regional Hygiene, Sanitation, and Epidemiology, Sci.-Pract. Conf., Abstracts of Papers), 1987, pp. 167–169.
Luzi, E. and Lopez-García, H.-M., Relative size variations in two vole species: a climatic proxy for the identification of humid-arid pulses during Late Pleistocene in Southwestern Europe?, Quat. Sci. Rev., 2019, vol. 223, p. 105920.
Luzi, E. and Lopez-García, H.-M., Patterns of variation in Microtus arvalis and Microtus agrestis populations from Middle to Late Pleistocene in southwestern europe, Hist. Biol., 2019a, vol. 31, no. 5, pp. 535–543.
Mačić, V., Albano, P.G., Almpanidou, V., Claudet, J., Corrales, X., Essl, F., Evagelopoulos, A., Giovos, I., Jimenez, C., Kark, S., Marković, O., Mazaris, A.D., Ólafsdóttir, G.A., Panayotova, M., Petović, S., Rabitsch, W., Ramdani, M., Rilov, G., and Tricarico, E., Vega Fernandez, T., Sini, M., Trygonis, V., and Katsanevakis, S., Biological invasions in conservation planning: a global systematic review, Front. Mar. Sci., 2018, vol. 5, p. 178.
Malygin, V.M., Baskevich, M.I., and Khlyap, L.A., Invasions of sibling species of the common vole, Ross. Zh. Biol. Invazii, 2019, no. 4, pp. 71–93.
Malyshev, Yu.S., On the issue of the formation of a new area of the range of the East European vole Microtus rossiaemeridionalis Ognev in Cisbaikalia, Baikal. Zool. Zh., 2013, no. 1 (12), pp. 105–108.
Maridet, O. and Ni, X., A new cricetid rodent from the Early Oligocene of Yunnan, China, and its evolutionary implications for early Eurasian cricetids, J. Vertebr. Paleontol., 2013, vol. 33, no. 1, pp. 185–194.
Markova, E.A., Assessing the complexity of the cheek teeth of voles (Arvicolinae, Rodentia): a ranked morphotypic approach, Zool. Zh., 2013, vol. 92, no. 8, pp. 968–980.
Markova, E. and Smirnov, N., Phenotypic diversity arising from a limited number of founders: a study of dental variation in laboratory colonies of collared lemmings, Dicrostonyx (Rodentia: Arvicolinae), Biol. J. Linn. Soc., 2018, vol. 125, pp. 777–793.
Markova, E.A., Malygin, V.M., Montuire, S., Nadachowski, A., Quéré, J.-P., and Ochman, K., Dental variation in sibling species Microtus arvalis and M. rossiaemeridionalis (Arvicolinae, Rodentia): between-species comparisons and geography of morphotype dental patterns, J. Mamm. Evol., 2010, vol. 17, pp. 121–139.
Markova, E.A., Yalkovskaya, L.E., and Zykov, S.V., Morphological and chromosomal variation in the common vole Microtus arvalis Pall. at the northern boundary of its distribution area, Dokl. Akad. Nauk, 2013, vol. 448, pp. 13–16.
Markova, E.A., Sibiryakov, P.A., Kartavtseva, I.V., Lapin, A.S., Morozkina, A.V., Petukhov, V.A., Tiunov, M.P., and Starikov, V.P., What can an invasive species tell us about evolution? A study of dental variation in disjunctive populations of Microtus rossiaemeridionalis (Arvicolinae, Rodentia), J. Mamm. Evol., 2019, vol. 26, no. 2, pp. 267–282.
Markova, E., Bobretsov, A., Borodin, A., Rakitin, S., Sibiryakov, P., Smirnov, N., Yalkovskaya, L., and Zykov, S., The effects of population bottlenecks on dental phenotype in extant arvicoline rodents: implications for studies of the quaternary fossil record, Quat. Sci. Rev., 2020, vol. 228, p. 106045.
Meyer, M.N., Golenishchev, F.N., Radzhabli, S.I., and Sablina, O.V., Serye polevki (podrod Microtus) fauny Rossii i sopredel’nykh territorii (Gray Voles (Subgenus Microtus) of the Fauna of Russia and Adjacent Territories), St. Petersburg: Zool. Inst. Ross. Akad. Nauk, 1996.
Van Der Meulen, A.J., Middle Pleistocene smaller mammals from the Monte Pegalia (Orvieto, Italy), with special reference to the phylogeny of Microtus (Arvicolidae, Rodentia), Quaternaria, 1973, vol. 17, pp. 1–144.
Moroldoev, I.V. and Kartavtseva, I.V., New data on the invasion of the East European vole (Microtus rossiaemeridionalis) to the east of Ulan-Ude, Vestn. Buryat. Gos. Univ., Ser. Biol., Geogr., 2017, vol. 3, pp. 130–134.
Moroldoev, I.V., Sheremet’eva, I.N., and Kartavtseva, I.V., The first find of the East European vole (Microtus rossiaemeridionalis) in Buryatia, Ross. Zh. Biol. Invazii, 2017, no. 2, pp. 88–94.
Nadachowski, A., Late Quaternary Rodents of Poland with Special Reference to Morphotype Dentition Analysis of Voles, Warszawa: Panstwowe wydawnictwo naukowe, 1982.
Nekrutenko, A., Makova, K.D., Chesser, R.K., and Baker, R.J., Representational difference analysis to distinguish cryptic species, Mol. Ecol., 1999, vol. 8, pp. 1235–1237.
Obyknovennaya polevka: vidy-dvoiniki (Common Vole: Twin Species), Sokolov, V.E. et al., Eds., Moscow: Nauka, 1994.
Pantalacci, S., Chaumot, A., Benoît, G., Sadier, A., Delsuc, F., Douzery, E.J.P., and Laudet, V., Conserved features and evolutionary shifts of the EDA signaling pathway involved in vertebrate skin appendage development, Mol. Biol. Evol., 2008, vol. 25, no. 5, pp. 912–928.
Pavlova, S.V. and Tchabovsky, A.V., Presence of the 54-chromosome common vole (Mammalia) on Olkhon Island (Lake Baikal, East Siberia, Russia), and the occurrence of an unusual X-chromosome variant, Comp. Cytogenet., 2011, vol. 5, no. 5, pp. 433–440.
Popov, V.V., Mammals of the Irkutsk region (annotated list), Baikal. Zool. Zh., 2011, no. 1 (6), pp. 69–78.
Reig, O.A., A proposed unified nomenclature for the enameled components of the molar teeth of the Cricetidae (Rodentia), J. Zool., 1977, vol. 181, pp. 227–241.
Richardson, D.M. and Riccardi, A., Misleading criticisms of invasion science: a field guide, Diversity Distrib., 2013, vol. 19, pp. 1461–1467.
Rodrigues, H.G., Renaud, S., Charles, C., Poul, Y., Solé, F., Aguilar, J.-P., Michaux, J., Tafforeau, P., Headon, D., Jernvall, J., and Viriot, L., Roles of dental development and adaptation in rodent evolution, Nat. Commun., 2013, vol. 4, p. 2504.
Rörig, G. and Börner, C., Studien über das Gebiss mitteleuropäischer recenter Mäuse, Arbeit aus der Kaiserlichen Biologischen Anstalt für Land- und Forstwirtschaft, Berlin: Paul Parey-Springer, 1905, vol. 5, no. 2, pp. 35–96.
Seppala, M., Fraser, G.J., Birjandi, A.A., Xavier, G.M., and Cobourne, M.T., Sonic hedgehog signaling and development of the dentition, J. Dev. Biol., 2017, vol. 5, no. 2, p. 6.
Sherpa, S. and Després, L., The evolutionary dynamics of biological invasions: a multi-approach perspective, Evol. Appl., 2021, vol. 14, no. 6, pp. 1463–1484.
Swaegers, J., Mergeay, J., Therry, L., Larmuseau, M.H.D., Bonte, D., and Stoks, R., Rapid range expansion increases genetic differentiation while causing limited reduction in genetic diversity in a damselfly, Heredity, 2013, vol. 111, pp. 422–429.
Vegetation cover of the Irkutsk region, 2013. http://irkipedia.ru/content/rastitelnyy_pokrov_atlas. Accessed March 20, 2023.
Wellcome Sanger Institute, Arvicola amphibius genome assembly mArvAmp1.2, 2021. www.ncbi.nlm.nih.gov/assembly/GCF_903992535.2. Updated May 15, 2021. Accessed April 25, 2023.
ACKNOWLEDGMENTS
The authors are grateful to A.V. Borodin for organizing cooperation and to O.V. Polyavina and A.O. Usoltseva for assistance at various stages of the study. The authors are also grateful to the anonymous reviewer for constructive comments.
Funding
This work was carried out within a State Assignment of the Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences, project no. 122021000094-3 (E.A. Markova, S.V. Zykov, L.E. Yalkovskaya, and S.V. Bulycheva).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
CONFLICT OF INTEREST
The authors of this work declare that they have no conflicts of interest.
Additional information
Translated by M. Shulskaya
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Markova, E.A., Borisov, S.A., Zykov, S.V. et al. Dental Variation in an Invasive Species at the Dispersal Stage: Microtus rossiaemeridionalis (Arvicolinae, Rodentia) in Irkutsk Oblast, Southern Cis-Baikal Region. Biol Bull Russ Acad Sci 50, 2538–2551 (2023). https://doi.org/10.1134/S1062359023090212
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1062359023090212