Phylogeography of ancient and modern brown bears from eastern Eurasia - PubMed (original) (raw)
. 2022 Feb 25;135(4):722-733.
doi: 10.1093/biolinnean/blac009. eCollection 2022 Apr.
Alexey I Makunin 1, Valentina V Salomashkina 2, Ilya G Kichigin 1, Nadezhda V Vorobieva 1, Sergey K Vasiliev 3, Mikhail V Shunkov 3, Alexey A Tishkin 4, Sergey P Grushin 4, Peeter Anijalg 5, Egle Tammeleht 5, Marju Keis 5, Gennady G Boeskorov 6, Nikolai Mamaev 7, Innokenty M Okhlopkov 7, Alexey P Kryukov 8, Elena A Lyapunova 9, Marina V Kholodova 2, Ivan V Seryodkin 10, Urmas Saarma 5, Vladimir A Trifonov 1, Alexander S Graphodatsky 1
Affiliations
- PMID: 35359699
- PMCID: PMC8943912
- DOI: 10.1093/biolinnean/blac009
Phylogeography of ancient and modern brown bears from eastern Eurasia
Anna S Molodtseva et al. Biol J Linn Soc Lond. 2022.
Abstract
The brown bear (Ursus arctos) is an iconic carnivoran species of the Northern Hemisphere. Its population history has been studied extensively using mitochondrial markers, which demonstrated signatures of multiple waves of migration, arguably connected with glaciation periods. Among Eurasian brown bears, Siberian populations remain understudied. We have sequenced complete mitochondrial genomes of four ancient (~4.5-40 kya) bears from South Siberia and 19 modern bears from South Siberia and the Russian Far East. Reconstruction of phylogenetic relationships between haplotypes and evaluation of modern population structure have demonstrated that all the studied samples belong to the most widespread Eurasian clade 3. One of the ancient haplotypes takes a basal position relative to the whole of clade 3; the second is basal to the haplogroup 3a (the most common subclade), and two others belong to clades 3a1 and 3b. Modern Siberian bears retain at least some of this diversity; apart from the most common haplogroup 3a, we demonstrate the presence of clade 3b, which was previously found mainly in mainland Eurasia and Northern Japan. Our findings highlight the importance of South Siberia as a refugium for northern Eurasian brown bears and further corroborate the hypothesis of several waves of migration in the Pleistocene.
Keywords: Denisova; ancient DNA; glacial refugium; mitochondrial genome; population structure.
© The Author(s) 2022. Published by Oxford University Press on behalf of The Linnean Society of London. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Figures
Figure 1.
Map of sample collection sites. Colour code: yellow, modern samples; red, ancient samples.
Figure 2.
BEAST phylogeny for complete mitochondrial genomes of 282 brown bears. Some subtrees have been collapsed for brevity. Red labels indicate ancient samples, and bold black labels indicate modern samples from the present study. Node numbers and blue lines are the mean and 95% confidence interval of divergence time (in thousands of years). Numbers over branches are the posterior Bayesian probabilities. Outgroups: India, Ursus thibetanus MG066704 and Ursus spelaeus NC_011112.
Figure 3.
Expanded view of clade 3 from Figure 2 representing phylogenetic placements of modern (shown in bold) and ancient (red) samples obtained in the present study. For labels of Published samples are described in Supporting Information (Table S3).
Figure 4.
Phylogenetic network of 136 modern bear mitochondrial genomes belonging to clades 3 and 4. Circle size corresponds to the number of identical samples. Colour code: yellow, Europe; blue, Siberia; green, Japan; red, Kamchatka; purple, the Russian Far East.
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References
- Anijalg P, Ho SYW, Davison J, Keis M, Tammeleht E, Bobowik K, Tumanov IL, Saveljev AP, Lyapunova EA, Vorobiev AA, Markov NI, Kryukov AP, Kojola I, Swenson JE, Hagen SB, Eiken HG, Paule L, Saarma U. 2018. Large-scale migrations of brown bears in Eurasia and to North America during the Late Pleistocene. Journal of Biogeography 45: 394–405.
- Barlow A, Cahill JA, Hartmann S, Theunert C, Xenikoudakis G, Fortes GG, Paijmans JLA, Rabeder G, Frischauf C, Grandal-d’Anglade A, García-Vázquez A, Murtskhvaladze M, Saarma U, Anijalg P, Skrbinšek T, Bertorelle G, Gasparian B, Bar-Oz G, Pinhasi R, Slatkin M, Dalén L, Shapiro B, Hofreiter M. 2018. Partial genomic survival of cave bears in living brown bears. Nature Ecology & Evolution 2: 1563–1570. - PMC - PubMed
- Barnes I, Matheus P, Shapiro B, Jensen D, Cooper A. 2002. Dynamics of Pleistocene population extinctions in Beringian brown bears. Science 295: 2267–2270. - PubMed
- Benazzo A, Trucchi E, Cahill JA, Maisano Delser P, Mona S, Fumagalli M, Bunnefeld L, Cornetti L, Ghirotto S, Girardi M, Ometto L, Panziera A, Rota-Stabelli O, Zanetti E, Karamanlidis A, Groff C, Paule L, Gentile L, Vilà C, Vicario S, Boitani L, Orlando L, Fuselli S, Vernesi C, Shapiro B, Ciucci P, Bertorelle G. 2017. Survival and divergence in a small group: the extraordinary genomic history of the endangered Apennine brown bear stragglers. Proceedings of the National Academy of Sciences of the United States of America 114: E9589–E9597. - PMC - PubMed
- Calvignac S, Hughes S, Tougard C, Michaux J, Thevenot M, Philippe M, Hamdine W, Hänni C. 2008. Ancient DNA evidence for the loss of a highly divergent brown bear clade during historical times. Molecular Ecology 17: 1962–1970. - PubMed
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