Genetic Diversity of the Field Vole Microtus agrestis (Arvicolinae, Rodentia) in the Central Part of Northern Eurasia According to the Cytochrome b Gene Data
- Authors: Yalkovskaya L.E.1, Sibiryakov P.A.2, Krohaleva M.A.1, Markova E.A.1, Borodin A.V.1, Borisov S.A.3, Chibiryak M.V.1, Bobretsov A.V.4
-
Affiliations:
- Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences
- Institute of Zoology of the Republic of Kazakhstan
- Irkutsk Antiplague Research Institute of Siberia and Far East
- Pechora-Ilych State Nature Reserve
- Issue: Vol 60, No 5 (2024)
- Pages: 51-65
- Section: ГЕНЕТИКА ЖИВОТНЫХ
- URL: https://rjpbr.com/0016-6758/article/view/667263
- DOI: https://doi.org/10.31857/S0016675824050041
- EDN: https://elibrary.ru/CJOZQK
- ID: 667263
Cite item
Abstract
An analysis of the genetic diversity of the field vole was carried out with the inclusion of new data on the complete sequences of the cytochrome b gene from the least studied area of the species range – the central part of Northern Eurasia (20 localities of the East European Plain, the Urals, Western and Eastern Siberia). The obtained results are generally consistent with modern view on the species phylogeography, but indicate the previously not investigated genetic heterogeneity of the Eastern clade, which occupies the entire Asian part of the species’ range and its European part to Northern and Eastern Europe. The comparison of the genetic diversity analysis results with the age of paleontological findings, carried out using the Urals territory as the example, allows to assume that climatic changes in the late Pleistocene and Holocene could not lead to the complete extinction of the species in the region, but to the spatial redistribution of its populations and to the complete or partial replacement of some genetic groups by others.
Full Text

About the authors
L. E. Yalkovskaya
Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences
Author for correspondence.
Email: lida@ipae.uran.ru
Russian Federation, Ekaterinburg
P. A. Sibiryakov
Institute of Zoology of the Republic of Kazakhstan
Email: lida@ipae.uran.ru
Kazakhstan, Almaty
M. A. Krohaleva
Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences
Email: lida@ipae.uran.ru
Russian Federation, Ekaterinburg
E. A. Markova
Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences
Email: lida@ipae.uran.ru
Russian Federation, Ekaterinburg
A. V. Borodin
Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences
Email: lida@ipae.uran.ru
Russian Federation, Ekaterinburg
S. A. Borisov
Irkutsk Antiplague Research Institute of Siberia and Far East
Email: lida@ipae.uran.ru
Russian Federation, Irkutsk
M. V. Chibiryak
Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences
Email: lida@ipae.uran.ru
Russian Federation, Ekaterinburg
A. V. Bobretsov
Pechora-Ilych State Nature Reserve
Email: lida@ipae.uran.ru
Russian Federation, Yaksha
References
- Млекопитающие России: систематико-географический справочник. М.: Т-во научн. изданий КМК, 2012. 604 с.
- Shenbrot G.I., Krasnov B.R. An Atlas of the Geographic Distribution of the Arvicoline Rodents of the World (Rodentia, Muridae: Arvicolinae). Sofia & Moscow: Pensoft Publ., 2005. 336 p.
- Kryštufek B., Vohralik V., Zima J., Zagorodnyuk I. Microtus agrestis (errata version published in 2017) // The IUCN Red List of Threatened Species. 2016. https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T13426A22349665.en
- Borodin A., Markova E., Zinovyev E. et al. Quaternary rodent and insect faunas of the Urals and Western Siberia: connection between Europe and Asia // Quat. Inter. 2013. V. 284. P. 132-150. https://doi.org/10.1016/j.quaint.2011.07.050
- Jaarola M., Searle J.B. A highly divergent mitochondrial DNA lineage of Microtus agrestis in southern Europe // Heredity. 2004. V. 92. P. 228–234.
- Paupério J., Herman J.S., Melo-Ferreira J. et al. Cryptic speciation in the field vole: A multilocus approach confirms three highly divergent lineages in Eurasia // Mol. Ecol. 2012. V. 21. P. 6015–6032. https://doi.org/10.1111/mec.12024
- Herman J.S., Stojak J., Paupério J. et al. Genetic variation in field voles (Microtus agrestis) from the British Isles: selective sweeps or population bottlenecks? // Biol. J. Linn. Soc. 2019. V. 126. № 4. P. 852–865. https://doi.org/10.1093/biolinnean/bly213
- Kryštufek B., Shenbrot G.I. Voles and Lemmings (Arvicolinae) of the Palaearctic Region. Univ. Maribor: Univ. Press, 2022. 437 p.
- Herman J.S., Searle J.B. Post-glacial partitioning of mitochondrial genetic variation in the field vole // Proc. R. Soc. B. 2011. V. 278. P. 3601–3607. https://doi.org/10.1098/rspb.2011.0321
- Herman J.S., McDevitt A.D., Kawałko A. et al. Land-bridge calibration of molecular clocks and the Post-Glacial colonization of Scandinavia by the eurasian field vole Microtus agrestis // PLoS One. 2014. V. 9. № 8. https://doi.org/10.1371/journal.pone.0103949
- Searle J.B., Kotlík P., Rambau R.V. et al. The Celtic fringe of Britain: Insights from small mammal phylogeography // Proc. R. Soc. B. 2009. V. 276. P. 4287–4294. https://doi.org/10.1098/rspb.2009.1422
- Beysard M., Perrin N., Jaarola M. et al. Asymmetric and differential gene introgression at a contact zone between two highly divergent lineages of field voles (Microtus agrestis) // J. Evol. Biol. 2012. V. 25. P. 400–408. https://doi.org/10.1111/j.1420-9101.2011.02432.x
- Stojak J., Borowik T., Górny M. et al. Climatic influences on the genetic structure and distribution of the common vole and field vole in Europe // Mammal. Res. 2018. V. 64. P. 19–29. https://doi.org/10.1007/s13364-018-0395-8
- Stojak J., Tarnowska E. Polish suture zone as the goblet of truth in post-glacial history of mammals in Europe // Mammal. Res. 2019. V. 64. P. 463–475. https://doi.org/10.1007/s13364-019-00433-6
- Равкин Ю.С., Богомолова И.Н., Шубилин С.М. и др. Пространственно-типологическая неоднородность населения мелких млекопитающих Западной Сибири (равнинная и горная территория) // Сиб. экол. журн. 2009. № 3. С. 475–487.
- Zinovyev E.V., Gilev A.V., Khantemirov R.M. Changes in the entomofauna of the southern Yamal Peninsula in connection with shifts of the northern timberline in the Holocene // Entomological Revi. 2001. V. 81. № 9. P. 1146–1152.
- Haynes S., Jaarola M., Searle J.B. Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago // Mol. Ecol. 2003. V. 12. P. 951–956. https://doi.org/10.1046/j.1365-294x.2003.01795.x
- Brunhoff C., Galbreath K.E., Fedorov V.B. et al. Holarctic phylogeography of the root vole (Microtus oeconomus): Implications for late Quaternary biogeography of high latitudes // Mol. Ecol. 2003. V. 12. P. 957–968. https://doi org/10.1046/j.1365-294x.2003.01796.x
- Сибиряков П.А., Товпинец Н.Н., Дупал Т.А. и др. Филогеография обыкновенной полевки Microtus arvalis (Rodentia, Arvicolinae) формы obscurus: новые данные по изменчивости митохондриальной ДНК // Генетика. 2018. Т. 54. № 10. С. 1162–1176. https://doi.org/10.1134/S0016675818100132
- Markova A.K., Puzachenko A.Yu., Glushankova N.I. The Likhvin (=Holsteinian, =Hoxnian) small mammal faunas of Europe (MIS 11) with reference to the easternmost Likhvin small mammal locality Rybnaya Sloboda (Volga basin, Russia) // Quat. Int. 2022. V. 674-675. P.18–30. https://doi.org/10.1016/j.quaint.2022.12.002
- Смирнов Н.Г., Большаков В.Н., Бородин А.В. Плейстоценовые грызуны севера Западной Сибири. М.: Наука, 1986. 146 с.
- Бородин А.В. Полевки (Arvicolinae, Rodentia) Урала и Западной Сибири (эоплейстоцен–голоцен): Дис. ... док. биол. наук. Екатеринбург: ИЭРиЖ УрО РАН, 2012. 585 с.
- Смирнов Н.Г. Разнообразие мелких млекопитающих Северного Урала в позднем плейстоцене и голоцене // Материалы и исследования по истории современной фауны Урала. Екатеринбург: Екатеринбург, 1996. С. 39–83.
- Kuzmina E.A., Smirnov N.G., Ulitko A.I. New data on Late Pleistocene–Holocene small mammal communities from the Ural–Sakmara interfluve, Southern Urals // Quat. Int. 2016. V. 420. P. 56–64. https://doi.org//10.1016/j.quaint.2016.02.007
- Смирнов Н.Г., Большаков В.Н., Косинцев П.А. и др. Историческая экология животных гор Южного Урала. Свердловск: УрО АН СССР, 1990. 224 с.
- Смирнов Н.Г., Кузьмина Е.А., Коурова Т.П. Новые данные о грызунах Северного Урала в позднеледниковье // Биота Приуральской Субарктики в позднем плейстоцене и голоцене. Екатеринбург: 1999, С. 68–77.
- Смирнов Н.Г. Мелкие млекопитающие Среднего Урала в позднем плейстоцене и голоцене. Екатеринбург: Наука, Уральское отд., 1993. 62 с.
- Изварин Е.П. Формирование фауны мелких растительноядных млекопитающих западного склона Среднего Урала в позднем плейстоцене и голоцене: Автореф. дис. … канд. биол. наук. Екатеринбург: ИЭРиЖ УрО РАН, 2017. 20 с.
- Фадеева Т.В., Смирнов Н.Г. Мелкие млекопитающие Пермского Предуралья в позднем плейстоцене и голоцене. Екатеринбург: Гощицкий, 2008. 172 с.
- Jaarola M., Searle J.B. Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences // Mol. Ecol. 2002. V. 11. P. 2613–2621. https://doiorg/10.1046/j.1365-294x.2002.01639.x
- Liu Sh., Jin W., Liu Y. et al. Taxonomic position of Chinese voles of the tribe Arvicolini and the description of 2 new species from Xizang, China // J. Mammal. 2017. V. 98. № 1. P. 166–182. https://doi.org/10.1093/jmammal/gyw170
- Lissovsky A.A., Petrova T.V., Yatsentyuk S.P. et al. Multilocus phylogeny and taxonomy of East Asian voles Alexandromys (Rodentia, Arvicolinae) // Zool. Scr. 2018. V. 47. № 1. P. 9–20. https://doi.org/10.1111/zsc.12261
- Aljanabi S.M., Martinez I. Universal and rapid salt-extraction of high-quality genomic DNA for PCR-based techniques // Nucl. Acids Res. 1997. V. 25. P. 4692–4693. https://doi.org/10.1093/nar/25.22.4692
- Tougard C., Brunet–Lecomte P., Fabre M., Montuire S. Evolutionary history of two allopatric Terricola species (Arvicolinae, Rodentia) from molecular, morphological, and palaeontological data // Biol. J. Linn. Soc. 2008. V. 93. P. 309–323. https://doi.org/10.1111/j.1095-8312.2007.00926.x
- Hall T.A. Bio-Edit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT // Nucl, Acids Symp. Series. 1999. V. 41. P. 95–98.
- Tamura K., Peterson D., Peterson N. et al. MEGA6: Molecular evolutionary genetics analysis version 6.0 // Mol. Biol. Evol. 2013.V. 30. P. 2725–2729. https://doi.org/10.1093/molbev/mst197
- Ronquist F., Teslenko M., Van Der Mark P. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space // Systematic Biol. 2012. V. 61. P. 539–542. https://doi.org/10.1093/sysbio/sys029
- Nylander J.A.A. MrModeltest v2. Program distributed by the author. 2004. Evolutionary Biology Centre, Uppsala Univ.
- Bandelt H.-J., Forster P., Röhl A. Median-joining networks for inferring intraspecific phylogenies // Mol. Biol. Evol. 1999. V. 16. P. 37–48.
- Leigh J.W., Bryant D. POPART: Full-feature software for haplotype networkconstruction // Methods Ecol. Evol. 2015. V. 6. P. 1110–1116. https://doi.org/10.1111/2041-210X.12410
- Excoffier L., Laval G., Schneider S. Arlequin (version 3.0): An integrated software package for population genetics data analysis // Evol. Bioinformatics Online. 2005. V. 1. P. 47–50. https://doi.org/10.1177/117693430500100003
- Librado P., Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data // Bioinformatics. 2009. V. 25. P. 1451–1452. https://doi.org/10.1093/bioinformatics/btp187
- Бердюгин К.И., Большаков В.Н., Балахонов В.С. и др. Млекопитающие Полярного Урала. Екатеринбург: изд-во Уральского ун-та, 2007. 384 с.
- Бобрецов А.В. Популяционная экология мелких млекопитающих равнинных и горных ландшафтов северо-востока Европейской части России. М.: Т-во науч. изданий КМК, 2016. 381 с.
- Кривцов В.А., Водорезов А.В. Физическая география и ландшафты России. Электронное учебное пособие. Рязань: Изд-во РГУ им. С.А. Есенина, 2016. 408 с.
- Абрамсон Н.И., Родченкова Е.Н., Костыгов А.Ю. Генетическая изменчивость и филогеография рыжей полевки (Clethrionomys glareolus, Arvicolinae, Rodentia) на территории России с анализом зоны интрогреcсии мтДНК близкородственного вида красной полевки (Сl. rutilus) // Генетика. 2009. Т. 45. № 5. С. 610–623. https://doi.org/10.1134/S1022795409050044
- Melnikova (Rodchenkova) E.N., Kshnyasev I.A., Bodrov S.Yu. et al. Sympatric area of Myodes glareolus and M. rutilus (Rodentia, Cricetidae): historic and recent hybridization// Proc. Zool. Institute RAS. 2012. V. 316. № 4. P. 307–323.
- Kobashi T., Severinghausa J.P., Brook E.J. et al. Precise timing and characterization of abrupt climate change 8200 years ago from air trapped in polar ice // Quat. Sci. Rev. 2007. V. 26. № 9–10. P. 1212–1222. https://doi.org/10.1016/j.quascirev.2007.01.009
- Li C., Li Y.-X., Zheng Y. et al. A high-resolution pollen record from East China reveals large climate variability near the Northgrippian-Meghalayan boundary (around 4200 years ago) exerted societal influence // Palaeogeography, Palaeoclimatology, Palaeoecology. 2018. V. 512. С. 156–165. https://doi.org/10.1016/j.palaeo.2018.07.031
- Markova E.A., Strukova T.V., Borodin A.V. Can we infer humidity gradients across the Ural Mountains during the Late Quaternary using Arvicoline rodents as an Environmental Proxy? // Rus. J. Ecol. 2022. V. 53. № 6. P. 485–499. https://doi.org/10.1134/s1067413622060108
Supplementary files
