Analysis of “historical” DNA of museum samples resolve taxonomic, nomenclature and biogeography issues: case study of true lemmings

Nataliya Abramson; Tatyana Petrova; Nikolay Dokuchaev

doi:10.21638/spbu03.2022.408

Authors

Nataliya Abramson Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, 199034, Saint Petersburg, Russian Federation https://orcid.org/0000-0003-3740-1388
Tatyana Petrova Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, 199034, Saint Petersburg, Russian Federation https://orcid.org/0000-0001-6856-920X
Nikolay Dokuchaev Institute of Biological Problems of the North, Far East Branch of the Russian Academy of Sciences, ul. Portovaya, 18, 685000, Magadan, Russian Federation https://orcid.org/0000-0002-1331-4901

DOI:

https://doi.org/10.21638/spbu03.2022.408

Abstract

Historical DNA of museum specimens is of paramount importance in elucidation of complex nomenclature issues and a priceless source of material gathered during preceding centuries in hardly accessible today sites. Here we report the results of genotyping type specimens of Lemmus obensis bungei Vinogradov, 1925 from the collection of the Zoological Institute RAS and specimens of lemmings from the upper streams of the Omolon River, identified as L. amurensis from the collection of the Institute of Systematics and Ecology of Animals, Siberian branch of RAS. The genetic profile of the type specimens in the first case was crucial for the nomenclatural solution as these specimens are from the point of the major evolutionary divergence on the Lena River. The results of the study convincingly showed that the lectotype belong to the eastern mitochondrial lineage of L. sibiricus. Therefore, if ever in the further studies it would be conclusively shown that this mitochondrial lineage may become a valid taxon of any rank, then names “novosibiricus”, “ognevi”, “portenkoi” will become younger synonyms of “bungei”. The new obtained sequences of the specimens from the Omolon prove initially wrong assignment and represent L. sibiricus eastern lineage.

Keywords:

historical DNA, collection samples, Lemmus, type specimens, cytochrome b, species identification

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References

Abramson, N. I., Kostygov, A. Yu., and Rodchenkova, E. N. 2008. The taxonomy and phylogeography of Palaearctic true lemmings (Lemmus, Cricetidae, Rodentia): new insights from cyt b data. Russian Journal Theriology 7:17–23. https://doi.org/10.15298/rusjtheriol.7.1.03

Abramson, N. I. and Lissovsky, A. A. 2012. Subfamily Arvicolinae; pp. 127–141 in I. Y. Pavlinov and A. A. Lissovsky (eds), The mammals of Russia: A taxonomic and geographic reference. KMK Scientific Press, Moscow.

Abramson, N. I. and Petrova, T. V. 2018. Genetic analysis of type material of the Amur lemming resolves nomenclature issues and creates challenges for the taxonomy of true lemmings (Lemmus, Rodentia: Cricetidae) in the eastern Palearctic. Zoological Journal of the Linnean Society 182(2):465–477. https://doi.org/10.1093/zoolinnean/zlx044

Abramson, N. I., Dokuchaev, N. E., and Petrova, T. V. 2018. Long-standing taxonomic and nomenclature issue of Lemmus obensis chrysogaster Allen, 1903 (Rodentia, Cricetidae) resolved. Mammalia 82(2):167–172. https://doi.org/10.1515/mammalia-2016-0081

Bandelt, H., Forster, P., and Röhl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16(1):37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

Baranova, G. I. and Gromov, I. M. 2003. Catalogue of type specimens in the collection of the Zoological Institute. Mammalia. No. 4. Rodentia. 100 pp. Izdatelstvo Zoologicheskogo instituta RAS, Saint Petersburg. (In Russian)

Carleton, M. D. and Musser, G. G. 2005. Order Rodentia; pp. 745–752 in D. E. Wilson and D. M. Reeder (eds), Mammal species of the world, 3rd ed. Johns Hopkins University Press, Baltimore.

Chernyavsky, F. B. 1984. The mammals of the extreme North-East Siberia. 388 pp. Nauka, Moscow. (In Russian)

Chernyavsky, F. B., Krivosheev, V. G., Revin, Yu. V., Khvorostyanskaya, L. P., and Orlov, V. N. 1980. On distribution, taxonomy and biology of the Amur lemming (Lemmus amurensis). Zoologichesky Zhurnal 59(7):1077–1084. (In Russian)

Chernyavsky, F. B., Abramson, N. I., Tsvetkova, A. A., Anbinder, E. M., and Kurysheva, L. P. 1993. On systematics and zoogeography of true lemming of the genus Lemmus (Rodentia, Cricetidae) of Beringia. Zoologichesky Zhurnal 72(8):111–122. (In Russian)

Chernyavsky, F. B. and Kartavtseva, I. V. 1999. On systematic status of lemmings (Rodentia, Cricetidae, Lemmus) from the Kolyma lowland. Zoologichesky Zhurnal 78(10):1237–1244. (In Russian)

Deffontaine, V., Libois, R., Kotlik, P., Sommer, R., Nieberding, C., Paradis, E., Searle, J. B., and Michaux J. R. 2005. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Molecular Ecology 14:1727–1739. https://doi.org/10.1111/j.1365-294X.2005.02506.x

Ellerman, J. R. and Morrison-Scott, R. C. S. 1951. Cheeklist of Palearctic and Indian Mammals. British Museum of Natural History, London.

Fedorov, V., Goropashnaya, A., Jarrell, G. H., and Fredga, K. 1999. Phylogeographic structure and mitochondria1 DNA variation in true lemmings (Lemmus) from the Eurasian Arctic. Biological Journal of the Linnean Society 66:357–371. https://doi.org/10.1111/j.1095-8312.1999.tb01896.x

Fedorov, V. B., Goropashnaya, A. V., Jaarola, M., and Cook, J. A. 2003. Phylogeography of lemmings (Lemmus): no evidence for postglacial colonization of Arctic from the Beringian refugium. Molecular Ecology 12:725–731. https://doi.org/10.1046/j.1365-294X.2003.01776.x

Fredga, K., Fedorov, V., Jarrell, G., and Jonson, L. 1999. Genetic diversity in Arctic Lemmings. AMBIO 28(3):261–269.

Gileva, E. A., Kuznetsova, I. A., and Cheprakov, M. I. 1984. Chromosome sets and taxonomy of the true lemmings (genus Lemmus). Zoologichesky Zhurnal 63:105–114. (In Russian)

Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98.

Hebert, P. D., Cywinska, A., Ball, S. L., and deWaard, J. R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences 270(1512):313–321. https://doi.org/10.1098/rspb.2002.2218

Hinton, M. A. C. 1926. Monograph of the voles and lemmings (Microtinae) living and extinct. British Museum Natural History, London. https://doi.org/10.5962/bhl.title.8319

Hoang, D. T, Chernomor, O., von Haeseler, A., Minh, B. Q., and Vinh, L. S. 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35:518–522. https://doi.org/10.1093/molbev/msx281

Jarrell, G. H. and Fredga, K. 1993. How many kinds of lemmings? A taxonomic overview; pp. 45–57 in N. C. Stenseth and R. A. Ims (eds), The Biology of Lemmings. Academic Press, London.

Kehlmaier, C., Zhang, X., Georges, A, Campbell, P. D., Thomson S., and Fritz, U. 2019. Mitogenomics of historical type specimens of Australasian turtles: clarification of taxonomic confusion and old mitochondrial introgression. Scientific Reports 9:5841. https://doi.org/10.1038/s41598-019-42310-x

Korsten, M., Ho, S. Y. W., Davison, J., Pähn, B., Vulla, E., Roht, M., Tumanov, I. L., Kojola, I., Andersone-Lilley, Z., Ozolins, J., Pilot, M., Mertzanis, Y., Giannakopoulos, A., Vorobiev, A. A., Markov, N. I., Saveljev, A. P., Lyapunova, E. A., Abramov, A. V., Männil, P., Valdmann, H., Pazetnov, S. V., Pazetnov, V. S., Rõkov, A. M., and Saarma, U. 2009. Sudden expansion of a single brown bear maternal lineage across northern continental Eurasia after the last ice age: a general demographic model for mammals? Molecular Ecology 18:1963–1979. https://doi.org/10.1111/j.1365-294X.2009.04163.x

Kostenko, V. A. 2000. Rodents (Rodentia) of the Russian Far East. 207 pp. Dalnauka Publ., Vladivostok. (In Russian)

Krystufek, B. and Shenbrot, G. I. 2022. Voles and Lemmings (Arvicolinae) of the Palaearctic Region. 449 pp. University Press, Maribor. https://doi.org/10.18690/um.fnm.2.2022

Kutschera, V. E., Bidon, T., Hailer, F., Rodi, J. L., Fain, S. R., and Janke, A. 2014. Bears in a forest of gene trees: phylogenetic inference is complicated by incomplete lineage sorting and gene flow. Molecular Biology and Evolution 31(8):2004–2017. https://doi.org/10.1093/molbev/msu186

Lagerholm, V. K., Sandoval-Castellanos, E., Ehrich, D., Abramson, N. I., Nadachowski, A., Kalthoff, D. C., Germonpré, M., Angerbjörn, A., Stewart, J. R., and Dalén, L. 2014. On the origin of the Norwegian lemming. Molecular Ecology 23:2060–2071. https://doi.org/10.1111/mec.12698

Lissovsky, A. A., Sheftel, B. I., Saveljev, A. P., Ermakov, O. A., Kozlov, Yu. A., Smirnov, D. G., Stakheev, V. V., and Glazov, D. M. 2019. Mammals of Russia: species list and applied issues. Archives of Zoological Museum of Moscow State University 56:1–191.

Ognev, S. I. 1948. Mammals of the USSR and Adjacent Territories. Vol. 6. Izdatelstvo Akademii nauk SSSR, Moskva–Leningrad. (In Russian)

Pavlinov, I. Ya. and Rossolimo, O. L. 1987. Systematics of mammals of the USSR. Moscow University Press, Moscow.

Pardiñas, U. F. J., Myers, P., León-Paniagua, L., Ordóñez Garza, N., Cook, J. A., Kryštufek, B., Haslauer, R., Bradley, R. D., Shenbrot, G. I., and Patton, J. L. 2017. Family Cricetidae (true hamsters, voles, lemmings and New World rats and mice); pp. 204–535 in D. E. Wilson, Jr. T. E. Lacher and R. A. Mittermeier (eds), Handbook of the mammals of the world. Vol. 7. Rodents II. Lynx Edicions, Barcelona.

Petrova, T. V., Tesakov, A. S., Kowalskaya, Y. M., and Abramson, N. I. 2016. Cryptic speciation in the narrowheaded vole, Lasiopodomys (Stenocranius) gregalis, (Rodentia: Cricetidae). Zoologica Scripta 45(6):618–629. https://doi.org/10.1111/zsc.12176

Pokrovski, A. V., Kuznetsova, I. A., and Cheprakov, M. I. 1984. Hybridological studies of reproductive isolation of the Lemmus Palearctic species (Rodentia, Cricetidae). Zoologichesky Zhurnal 63(6):904–911. (In Russian)

Raxworthy, C. J. and Smith, B. T. 2021. Mining museums for historical DNA: advances and challenges in museomics. Trends in Ecology & Evolution 36(11):1049–1060. https://doi.org/10.1016/j.tree.2021.07.009

Rausch, R. L. and Rausch, V. R. 1975. Taxonomy and zoogeography of Lemmus spp. (Rodentia, Arvicolinae) with notes on laboratory-reared lemmings. Ibidem 40:8–34.

Renner, S. S. 2016. A return to Linnaeus’s focus on diagnosis, not description: the use of DNA characters in the formal naming of species. Systematic Biology 65(6):1085–1095. https://doi.org/10.1093/sysbio/syw032

Shaw, K. L. 2002. Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: What mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. PNAS 99 (25):16122–16127. https://doi.org/10.1073/pnas.242585899

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

Spitsyn, V. M., Bolotov, I. N., Kondakov, A. V., Klass, A. L., Mizin, I. A., Tomilova, A. A., Zubrii, N. A., and Gofarov, M. Y. 2021. A new Norwegian Lemming subspecies from Novaya Zemlya, Arctic Russia. Ecologica Montenegrina 40:93–117. https://doi.org/10.37828/em.2021.40.8

Toews, D. P. and Brelsford, A. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21(16):3907–3930. https://doi.org/10.1111/j.1365-294X. 2012.05664.x

Trifinopoulos J., Nguyen L.-T., von Haeseler A., and Minh B. Q. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44: W232–W235. https://doi.org/10.1093/nar/gkw256

Vinogradov, B. S. 1924. Two new interesting lemmings from Siberia. The Annals and Magazine of Natural History 14:186–189. https://doi.org/10.1080/00222932408633106

Vinogradov, B. S. 1925. Materials on taxonomy and morphology of rodents. III. Notes on Palaearctic lemmings (genus Lemmus). Ezhegodnik Zoologicheskogo Museya AN SSSR 26:51–73. (In Russian)

Wandeler, P., Hoeck, P. E. A. and Keller, L. F. 2007. Back to the future: museum specimens in population genetics. Trends in Ecology & Evolution 22(12):634–642. https://doi.org/10.1016/j.tree.2007.08.017