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Genetic variability of Prunus padus (Rosaceae) elaborates “a new Eurasian phylogeographical paradigm”

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The extent of glacial survival of woody plants in temperate Asia is still poorly known. A reliable way to clarify this issue in the absence of sufficient paleontological data is a phylogeographic analysis of contemporary populations. A recent study of Juniperus communis genetic diversity in Eurasia suggested that this species with wide ecological tolerance survived the glaciation in many periglacial microrefugia at high latitudes and subsequently spread to new areas during interglacials (Hantemirova et al. in J Biogeogr 44:271–282, 2017. https://doi.org/10.1111/jbi.12867). This pattern was termed a “new Eurasian phylogeographical paradigm” as opposed to survival in few major refugia. We have tested the proposed “paradigm” with another hardy species with wide Eurasian area, Prunus padus, to find out if any general phylogeographic patterns may exist for cold-tolerant Eurasian arboreal plant species. We interpret the observed genetic structure [nuclear (ITS) and plastid DNA] of the Eurasian populations of P. padus as plausibly resulted from at least two cycles of glacial survivals in refugia followed by post-glacial colonization events. The species likely originated in East Asia and subsequently spread across all Eurasia. Its continuous range had been fragmented by early-Pleistocene glaciations, when the species survived in the Caucasian and Far Eastern refugia as well as in northern periglacial microrefugia with an active gene flow between them. The known major glacial refugia, such as Iberian Peninsula, the Colchis, the Southern Urals, and the Beringia, played little role as a source of the species post-glacial expansion.

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  1. Abellán P, Svenning JC (2014) Refugia within refugia—patterns in endemism and genetic divergence are linked to Late Quaternary climate stability in the Iberian Peninsula. Biol J Linn Soc 113:13–28. https://doi.org/10.1111/bij.12309

  2. Anijalg P, Ho SYW, Davison J et al (2018) Large-scale migrations of brown bears in Eurasia and to North America during the Late Pleistocene. J Biogeogr 45:394–405. https://doi.org/10.1111/jbi.13126

  3. Aradhya M, Velasco D, Ibrahimov Z et al (2017) Genetic and ecological insights into glacial refugia of walnut (Juglans regia L.). PLoS ONE 12:e0185974. https://doi.org/10.1371/journal.pone.0185974

  4. Arkhipov SA, Ehlers J, Johnson RG, Wright HE (1995) Glacial drainages towards the Mediterranean during middle age and late Pleistocene. Boreas 24:196–206. https://doi.org/10.1111/j.1502-3885.1995.tb00773.x

  5. Barkalov VYu, Taran AA (2004) List of vascular plant species of the Sakhalin island. In: Storozhenko SYu (ed) Flora and fauna of Sakhalin island (Materials of International Sakhalin Island Project), part 1. Dalnauka, Vladivostok, pp 39–66 (In Russian)

  6. Binney H, Edwards M, Macias-Fauria M et al (2017) Vegetation of Eurasia from the last glacial maximum to present: key biogeographic patterns. Quatrn Sci Rev 157:80–97. https://doi.org/10.1016/j.quascirev.2016.11.022

  7. Blokhina NI, Bondarenko OV (2011) Fossil plant assemblages from the Pliocene of southern Primory’e Region (Russian Far East): implications for reconstruction of plant communities and their environments. Acta Palaeobot. 51:19–37

  8. Brubaker LB, Anderson PM, Edwards ME (2005) Beringia as a glacial refugium for boreal trees and shrubs: new perspectives from mapped pollen data. J Biogeogr 32:833–848. https://doi.org/10.1111/j.1365-2699.2004.01203.x

  9. Buzunova IO (2001) Padus Miller. In: Tzvelev NN (ed) Flora of Eastern Europe, vol. 10. Izdatelstvo Sankt-Peterburgskoj khmiko-farmatsevticheskoj akademii, Saint-Petersburg, pp 594–596 (In Russian)

  10. Caudullo G, Welk E, San-Miguel-Ayanz J (2017) Chorological maps for the main European woody species. Data Brief 12:662–666. https://doi.org/10.1016/j.dib.2017.05.007

  11. Chiang T-Y, Schaal BA (2000) Molecular evolution and phylogeny of the atpB-rbcL spacer of chloroplast DNA in the true mosses. Genome 43:417–426

  12. Chin S-W, Shaw J, Haberle R, Wen J, Potter D (2014) Diversification of almonds, peaches, plums and cherries—molecular systematics and biogeographic history of Prunus (Rosaceae). Molec Phylogen Evol 76:34–48. https://doi.org/10.1016/j.ympev.2014.02.024

  13. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x

  14. Connor SE, Kvavadze EV (2009) Modelling late Quaternary changes in plant distribution, vegetation and climate using pollen data from Georgia, Caucasus. J Biogeogr 36:529–545. https://doi.org/10.1111/j.1365-2699.2008.02019.x

  15. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

  16. Eidesen PB, Ehrich D, Bakkestuen V, Alsos IG, Gilg O, Taberlet P, Brochmann C (2013) Genetic roadmap of the arctic: plant dispersal highways, traffic barriers and capitals of diversity. New Phytol 200:898–910. https://doi.org/10.1111/nph.12412

  17. Fisyun VV (1961) Padus Mill. In: Pavlov NV (ed) Flora of Kazakhstan, vol. 4. Kazakh Academy of Sciences, Alma-Ata, pp 516–518 (In Russian)

  18. Gladkova VN (1984) Padus Mill. In: Yurtsev BA (ed) Arctic flora of the USSR, vol. 9(1). Nauka, Saint-Petersburg, pp 306–308 (In Russian)

  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

  20. Hantemirova EV, Heinze B, Knyazeva SG et al (2017) A new Eurasian phylogeographical paradigm? Limited contribution of southern populations to the recolonization of high latitude populations in Juniperus communis L. (Cupressaceae). J Biogeogr 44:271–282. https://doi.org/10.1111/jbi.12867

  21. Herden T, Hanelt P, Friesen N (2016) Phylogeny of Allium L. subgenus Anguinum (G. Don. ex W.D.J. Koch) N. Friesen (Amaryllidaceae). Molec Phylogen Evol 95:79–93. https://doi.org/10.1016/j.ympev.2015.11.004

  22. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molec Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030

  23. Ikeda H, Yoneta Y, Higashi H, Eidesen PB, Barkalov V, Yakubov V, Brochmann C, Setoguchi H (2015) Persistent history of the bird-dispersed arctic-alpine plant Vaccinium vitis-idaea L. (Ericaceae) in Japan. J Pl Res 128:437–444. https://doi.org/10.1007/s10265-015-0709-8

  24. Jakob SS, Blattner FR (2006) A chloroplast genealogy of Hordeum (Poaceae): long term persisting haplotypes, incomplete lineage sorting, regional extinction, and the consequences for phylogenetic inference. Molec Biol Evol 23:1602–1612. https://doi.org/10.1093/molbev/msl018

  25. Kadyrov GM (1954) Padus Mill. In: Karyagin II (ed) Flora of Azerbaijan, vol. 5. Academy of Sciences of Azerbaijan, Baku, p 196

  26. Kamelin RV, Ovesnov SA, Shilova SI (1999) Broad-leaved forest refugia of the Urals and Altai. In: Khlebnikova LV (ed) Nemoral elements in floras of Ural and Siberia. University Perm, Perm, pp 18–26 (In Russian)

  27. Komarov VL (1941) Padus Mill. In: Komarov VL (ed) Flora of the USSR, vol. 10. Academy of Sciences, Saint-Petersburg, Moscow, pp 575–579 (In Russian)

  28. Kosintsev PA, Lapteva EG, Korona OM, Zanina OG (2012) Living environments and diet of the Mongochen mammoth, Gydan Peninsula. Russia. Quatern Int 276–277:253–268. https://doi.org/10.1016/j.quaint.2011.11.004

  29. Ku T-C, Bartholomew B (2003) Padus Miller. In: Wu Z, Raven P (eds) Flora of China, vol. 9. Science Press & Missouri Botanical Garden Press, St. Louis, Beijing, pp 420–426

  30. Leather SR (1996) Prunus padus L. J Ecol 84:125–132

  31. Liu X-L, Wen J, Nie Z-L, Yang C-Z (2012) Polyphyly of the Padus group of Prunus (Rosaceae) and the evolution of biogeographic disjunctions between eastern Asia and eastern North America. J Pl Res 126:351–361. https://doi.org/10.1007/s10265-012-0535-1

  32. Logan SA, Chytry M, Wolff K (2018) Genetic diversity and demographic history of the Siberian lime (Tilia sibirica). Perspect Pl Ecol 33:9–17. https://doi.org/10.1016/j.ppees.2018.04.005

  33. Nedoluzhko VA (1996) Padus Mill. In: Kharkevich SS (ed) Vascular plants of the Russian Far East, vol. 8. Nauka, Saint-Petersburg, pp 235–239 (In Russian)

  34. Nikitin VP (2006) Paleocarpology and issues of stratigraphy of Neogene of Western Siberia. Geol Geophys 47:963–970 (In Russian)

  35. Ovchinnikova SV (2012) Padus Mill. In: Baikov KS (ed) Annotated checklist of flora of Asian Russia: vascular plants. Siberian branch RAS, Novosibirsk, p 225

  36. Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

  37. R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/

  38. Semerikov VL, Semerikova SA, Polezhaeva MA, Kosintsev PA, Lascoux M (2013) Southern montane populations did not contribute to the recolonization of West Siberian Plain by Siberian larch (Larix sibirica): a range-wide analysis of cytoplasmic markers. Molec Ecol 22:4958–4971. https://doi.org/10.1111/mec.12433

  39. Semerikov VL, Semerikova SA, Putintseva YA et al (2018) Colonization history of Scots pine in Eastern Europe and North Asia based on mitochondrial DNA variation. Tree Genet Genomes 14:8. https://doi.org/10.1007/s11295-017-1222-0

  40. Seregin A (ed) (2018) Moscow University Herbarium (MW). Version 1.51. Lomonosov Moscow State University. Occurrence Dataset. Available at: https://doi.org/10.15468/cpnhcc. Accessed 24 Oct 2018

  41. Shaw J, Lickey E, Beck JT et al (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast sequences for phylogenetic analysis. Amer J Bot 92:142–166. https://doi.org/10.3732/ajb.92.1.142

  42. Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Amer J Bot 94:275–288. https://doi.org/10.3732/ajb.94.3.275

  43. Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–613. https://doi.org/10.1016/S0169-5347(01)02338-2

  44. Svendsen JI, Alexanderson H, Astakhov VI et al (2004) Late Quaternary ice sheet history of northern Eurasia. Quatern Sci Rev 23:1229–1271. https://doi.org/10.1016/j.quascirev.2003.12.008

  45. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/BF00037152

  46. Taberlet P, Fumagalli L, Wust-Saucy AG, Cossons J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molec Ecol 7:453–464. https://doi.org/10.1046/j.1365-294x.1998.00289.x

  47. Tarkhnishvili D, Gavashelishvili A, Mumladze L (2012) Palaeoclimatic models help to understand current distribution of Caucasian forest species. Biol J Linn Soc 105:231–248. https://doi.org/10.1111/j.1095-8312.2011.01788.x

  48. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

  49. Teodoris V, Kvaček Z, Uhl D (2009) Pliocene palaeoenvironment and correlation of the Sessenheim-Auenheim floristic complex (Alsace, France). Palaeodiversity 2:1–17

  50. Vakhrameeva MG (1975) Padus avium Mill. In: Rabotnov TA (ed) Biological Flora of Moscow region, vol. 2. Moscow State University, Moscow, pp 81–88 (In Russian)

  51. Velichko AA, Timireva SN, Kremenetski KV, MacDonald GM, Smith LC (2011) West Siberian Plain as a late glacial desert. Quatern Int 237:45–53. https://doi.org/10.1016/j.quaint.2011.01.013

  52. Volkova PA, Schanzer IA, Soubani E, Meschersky IG, Widen B (2016) Phylogeography of the European rock rose Helianthemum nummularium (Cistaceae): western richness and eastern poverty. Pl Syst Evol 302:781–794. https://doi.org/10.1007/s00606-016-1299-1

  53. Vydrina SN (1988) Padus Mill. In: Polozhev AV, Malysheva LI (eds) Flora of Siberia, vol. 8. Nauka, Novosibirsk, p 130 (In Russian)

  54. Wang Z, Zeng Y, Zhang Z, Sheng S, Tian J, Wu R, Pang X (2017) Phylogeography study of the Siberian apricot (Prunus sibirica L.) in Northern China assessed by chloroplast microsatellite and DNA markers. Fronties Pl Sci 8:1989. https://doi.org/10.3389/fpls.2017.01989

  55. Wen J, Zimmer E (1996) Phylogeny and biogeography of Panax L. (the ginseng genus, Araliaceae): inferences from ITS sequences of nuclear ribosomal DNA. Molec Phylogen Evol 6:167–177. https://doi.org/10.1006/mpev.1996.0069

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We thank all the collectors who provided herbarium and silica gel samples: L. Abramova, L. Adamec, J. Calvo, T. Fukuda, E. Chemeris, M. Grigoryan, M. Ivanova, Yu. Kopylov-Guskov, E. Hantemirova, C. Kim, M. Kropf, R. Murtazaliev, A. Mustafina, M. Nosova, E. Pimenova, N. Reshetnikova, C. Romero Redriguez, G. Sramko, N. Tikhomirov, B. Widen, T. Voronkova, D. Zakharchenko. We are grateful to T. Nagamitsu for the information on the distribution of Padus ssiori in Japan and Yu. Bykov for the English correction. Some material was collected at the “Lake Moldino” biological station of the South-West School # 1543, during a field student training course of the Lomonosov Moscow State University and at the territories of Baikalsky, Kandalakshsky, Nizhnesvirsky, and Orenburgsky State nature reserves; we thank their staff for cooperation. We are also grateful to the administration of Verkhnedonskoj district of Rostov Province of the Russian Federation for the help during the student field training in 2018.


This work was partly supported by the Russian Fund for Basic Research (Grant Number 15-29-02486-ofi_m), Tsitsin Main Botanical Garden state assignment (Number 19-119012390082-6), and the Moscow Department of Education.

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Correspondence to Polina A. Volkova.

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Online Resource 1. Geographical origin, ITS ribotypes, and cpDNA haplotypes of the studied populations of the Prunus spp.

Online Resource 2. The maximum likelihood tree for the observed haplotypes.

Online Resource 3. The maximum likelihood tree for the observed ribotypes.

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Volkova, P.A., Burlakov, Y.A. & Schanzer, I.A. Genetic variability of Prunus padus (Rosaceae) elaborates “a new Eurasian phylogeographical paradigm”. Plant Syst Evol 306, 1 (2020). https://doi.org/10.1007/s00606-020-01644-0

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  • Arboreal vegetation
  • Beringia
  • Colchis
  • Criptic refugia
  • Eurasia
  • Glacial survival