Is Betula carpatica genetically distinctive? A morphometric, cytometric and molecular study of birches in the Bohemian Massif with a focus on Carpathian birch


Autoři: Ivan Kuneš aff001;  Rostislav Linda aff001;  Tomáš Fér aff002;  Petr Karlík aff003;  Martin Baláš aff001;  Jana Ešnerová aff001;  Jan Vítámvás aff003;  Jan Bílý aff004;  Tomáš Urfus aff002
Působiště autorů: Department of Silviculture, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Czech Republic aff001;  Department of Botany, Faculty of Science, Charles University, Prague, Czech Republic aff002;  Department of Forest Ecology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Czech Republic aff003;  EXTEMIT-K, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Czech Republic aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224387

Souhrn

Until recently, Czech taxonomists often treated Betula carpatica as a distinct species. Several morphological traits for distinguishing B. carpatica from B. pubescens or other birches are described in literature; however, it has been proven impossible to reliably identify B. carpatica in the field. With the use of morphological and molecular approaches, we intended to assess the position of B. carpatica in the context of other birch taxa reported from the Bohemian Massif and to find more reliable morphological traits for their identification. In our dataset, we distinguished the following birch taxa referred to in the recent Czech literature: B. pendula, B. pubescens, B. carpatica, B. oycoviensis, B. nana, B. petraea and B. ×seideliana. We complemented them with triploids and several diploid and tetraploid “working units” into which we included intermediate individuals that in terms of morphology did not unambiguously match any of the abovementioned birch taxa. Holoploid genome size was measured to determine the ploidy level. To identify genetic relationships between selected taxa and “working units”, microsatellite analyses were performed. Model-based STRUCTURE analysis together with principal coordinates analysis (PCoA) based on genetic distances was performed to identify the similarities in multilocus genotype data between groups distinguished in the dataset. The applied analyses were not able clearly to distinguish any group among tetraploid individuals. In this light, it was of no use to search for any more reliable morphological traits of B. carpatica and also B. petraea. Among diploids, B. nana was always distinguished, in contrast to B. oycoviensis, which was not genetically recognized despite being usually morphologically distinct. Based on our results and a literature review, we suggest that B. carpatica and also the closely similar B. petraea should not be considered separate species. A similar conclusion seems relevant also for B. oycoviensis; however, further verification is desirable in this case.

Klíčová slova:

Birches – Flow cytometry – Leaves – Species delimitation – Taxonomy – Triploidy – Tetraploidy – Ploidy


Zdroje

1. Furlow JJ. The genera of Betulaceae in the southeastern United States. Journal of the Arnold Arboretum. 1990;71:1–67. doi: 10.5962/bhl.part.24925

2. Chen Z-D, Manchester SR, Sun H-Y. Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology and paleobotany. Am J Bot. 1999;86(8):1168–81. 10449397

3. Järvinen P, Palmé A, Morales LO, Läännenpää M, Kenänen M, Sopanen T, et al. Phylogenetic relationship of Betula species (Betulaceae) based on nuclear ADH and chloroplast matK chronosequence. Am J Bot. 2004;91(11):1834–45. doi: 10.3732/ajb.91.11.1834 21652331

4. Bina H, Yousefzadeh H, Ali SS, Esmailpour M. Phylogenetic relationships, molecular taxonomy, biogeography of Betula, with emphasis on phylogenetic position of Iranian populations. Tree Genet Genomes. 2016;12(5):17. doi: 10.1007/s11295-016-1037-4

5. Atkinson MD. Betula pendula Roth (B. Verrucosa Ehrh.) and B. Pubescens Ehrh. Journal of Ecology. 1992;80(4):837–70. doi: 10.2307/2260870

6. Howland DE, Oliver RP, Davy AJ. Morphological and molecular variation in natural populations of Betula. New Phytol. 1995;130(1):117–24.

7. Schenk MF, Thienpont C-N, Koopman WJM, Gilissen LJWJ, Smulders MJM. Phylogenetic relationships in Betula (Betulaceae) based on AFLP markers. Tree Genet Genomes. 2008;4(4):911–24. doi: 10.1007/s11295-008-0162-0

8. Roy NS, Lee S-I, Nkongolo K, Kim N-S. Retrotransposons in Betula nana, and interspecific relationships in the Betuloideae, based on inter-retrotransposon amplified polymorphism (IRAP) markers. Genes & Genomics. 2018;40(5):511–9. doi: 10.1007/s13258-018-0655-7 29892962

9. Ashburner K, McAllister HA. The genus Betula: a taxonomic revision of birches: Royal Botanic Gardens Kew; 2013. 431 p.

10. Grimm GW, Renner SS. Harvesting Betulaceae sequences from GenBank to generate a new chronogram for the family. Bot J Linnean Soc. 2013;172(4):465–77. doi: 10.1111/boj.12065

11. Elkington TT. Itrogressive hybridization between Betula nana L. and B. pubescens Ehrh. in north-west Iceland. New Phytol. 1968;67(1):109–18. doi: 10.1111/j.1469-8137.1968.tb05459.x

12. Wang N, McAllister HA, Bartlett PR, Buggs RJA. Molecular phylogeny and genome size evolution of the genus Betula (Betulaceae). Ann Bot (London). 2016;117(6):1023–35. doi: 10.1093/aob/mcw048 27072644

13. Anamthawat-Jónsson K, Thór Thórsson A. Natural hybridisation in birch: triploid hybrids between Betula nana and B. pubescens. Plant Cell, Tissue and Organ Culture. 2003;75(2):99–107. doi: 10.1023/a:1025063123552

14. Palme AE, Su Q, Palsson S, Lascoux M. Extensive sharing of chloroplast haplotypes among European birches indicates hybridization among Betula pendula, B. pubescens and B. nana. Molecular Ecology. 2004;13(1):167–78. doi: 10.1046/j.1365-294x.2003.02034.x 14653797

15. Thomson AM, Dick CW, Dayanandan S. A similar phylogeographical structure among sympatric North American birches (Betula) is better explained by introgression than by shared biogeographical history. Journal of Biogeography. 2015;42(2):339–50. doi: 10.1111/jbi.12394

16. Brown IR, Al-Dadwoody D. Obseravations on meiosis in three cytotypes of Betula alba L. New Phytol. 1979;83(3):801–11. doi: 10.1111/j.1469-8137.1979.tb02311.x

17. McAllister H, Ashburner K. 593. Betula megrelica. Curtis’s Botanical Magazine. 2007;24:174–9. doi: 10.1111/j.1467-8748.2007.00582.x

18. Skokanová K. Rod Betula L. na Slovensku (diplomová práca). Bratislava: Univerzita Komenského V Bratislave, Prirodovedecká fakulta, katedra botaniky; 2003. 89 p.

19. Eifler I. Untersuchungen zur individuellen Bedingtheit des Kreuzungserfolges zwischen Betula pendula und Betula pubescens Silvae Genetica. 1960;9:159–65.

20. Brown IR, Kennedy D, Williams P. The occurrence of natural hybrids between Betula pendula Roth and B. pubescens Ehrh. Watsonia. 1982;14:133–45.

21. Gausmann P, Goetz Heinrich L. Morphologie und variationsbreite der bastard-birke (Betula ×aurata Borkh., Betulaceae) auf urban- industriell geprägten standorten im ruhrgebiet. Floristische Rundbriefe. 2014;46:95–116.

22. Jadwiszczak KA. What can molecular markers tell us about the glacial and postglacial histories of European birches? Silva Fenn. 2012;46(5):733–45.

23. Franiel I. Taxonomic problems of Betula obscura (Betulaceae). A review. Fragmenta Floristica et Geobotanica Polonica. 2009;16(1):27–32.

24. Walters SM. Betula L. 1993. In: Flora Europaea [Internet]. Cambridge: Cambridge University Press. 2nd. [68–9].

25. Väre H. Mountain birch taxonomy and floristics of mountain birch woodlands. 2001. In: Nordic mountain birch ecosystems [Internet]. Paris New York London: UNESCO Parthenon Publishing Group; [35–46].

26. Sýkora T. Taxonomie a rozšíření bříz okruhu Betula alba v Českém masívu. Zprávy Československé botanické společnosti. 1983;18(1):1–14.

27. Domin K. Betula atrata Domin, nová bříza z Českomoravské vysočiny. Rozpravy České akademie věd a umění. 1927;36(52):1–10.

28. Vašut R. Betula L. In: Kaplan Z, editor. Klíč ke květeně České republiky [Key to the flora of the Czech Republic; revised and updated edition]. Praha: Academia; 2019. p. 536–8.

29. Natho G. Variationsbreite und Bastardbildung bei mitteleuropäischen Birkensippen. Repertorium novarum specierum regni vegetabilis. 1959;61(3):211–73. doi: 10.1002/fedr.19590610304

30. Szafer W, Kulczyński S, Pawłowski B. Rośliny Polskie. Warszawa, Poland: Państwowe Wydawnictwo Naukowe; 1967. 1020 p.

31. Pawlowska L. Flavonoids in the leaves of Polish species of the genus Betula L. IV. The flavonoids of Betula pubescens Ehrh., B. carpatica Waldst., B. tortuosa Ledeb., and B. nana L. leaves. Acta Soc Bot Pol. 1982;51(3–4):403–11.

32. Pawlowska L. Biochemical and systematic study of the genus Betula L. Acta Scientatis Botanicorum Poloniae. 1983;52(3–4):301–3014. doi: 10.5586/asbp.1983.034

33. Gardiner AS. A review of the sub-species carpatica and tortuosa within the species Betula pubescens Ehrh. Transactions of the Botanical Society of Edinburgh. 1972;41(4):451–9. doi: 10.1080/03746607208685245

34. Christensen KI. De Skandinaviske Birke [The Scandinavian birches]. Dansk Dendrologist Årsskrift. 1983;6(1):22–36.

35. Blackmore S, Steinmann JAJ, Hoen PP, Punt W. BETULACEAE and CORYLACEAE. Review of Palaeobotany and Palynology. 2003;123(1–2):71–98. http://dx.doi.org/10.1016/S0034-6667(02)00156-2.

36. Fischer MA, Oswald K, Adler W, editors. Exkursionsflora für Österreich, Liechtenstein und Südtirol. 2nd ed. Linz, Österreich: Oberösterreichisches Landesmuseum Linz; 2005.

37. Goliašová K, Michalková E, editors. Flóra Slovenska V/3. Bratislava, Slovakia: VEDA, vydavatel’stvo SAV; 2006.

38. Jäger E, editor. Rothmaler—Exkursionsflora von Deutschland. Gefäßpflanzen: Grundband. 21st ed. Berlin, Heidelberg: Springer Spektrum; 2017.

39. Rutkowski L. Klucz do oznaczania roślin naczyniowych Polski niżowej. Warszawa: Wydawnictwo Naukowe PWN 2018. 816 p.

40. Li JH, Shoup S, Chen ZD. Phylogenetics of Betula (Betulaceae) inferred from sequences of nuclear ribosomal DNA. Rhodora. 2005;107(929):69–86. doi: 10.3119/04-14.1

41. Poland J, Clement E. The Vegetative Key to the British Flora: A new approach to naming British vascular plants based on vegetative characters. London: Poland John, Southampton, in association with the Botanical Society of the British Isles 2009. 556 p.

42. Kříž Z, editor Betula L.–bříza. Květena České republiky, 2; 2003: Academia, Praha.

43. Kubát K, Hrouda L, Chrtek J, Kaplan Z, Kirschner J, Štěpánek J. Klíč ke květeně České repubiky [Key to the Flora of the Czech Republic]. Praha: Academia; 2002. 928 p.

44. Balcar V. Some experience of European birch (Betula pendula Roth) and Carpathian birch (Betula carpatica W. et K.) planted on the ridge part of the Jizerské hory Mts. J For Sci. 2001;47(Special Issue):150–5.

45. Úradníček L, Maděra P, Tichá S, Koblížek J. Dřeviny České republiky. Kostelec nad Černými lesy: Lesnická práce 2009. 368 p.

46. Kuneš I, Baláš M, Ešnerová J, Koňasová T, Vítámvás J, Zahradník D, et al., editors. Bříza byla a zůstává tématem pro lesnický provoz i výzkum. Bříza—strom roku 2010; 2010; Kostelec nad Černými lesy: Česká zemědělská univerzita v Praze.

47. Chytrý M, Kučera T, Kočí M, Grulich V, Lustyk P, editors. Katalog biotopů České republiky [Habitat Catalogue of the Czech Republic]. 2nd ed. Praha: Agentura ochrany přírody a krajiny ČR; 2010.

48. Viewegh J, Kusbach A, Mikeska M. Czech forest ecosystem classification. J For Sci. 2003;49(2):85–93.

49. Linda R, Kuneš I, Baláš M, Gallo J. Morphological variability between diploid and tetraploid taxa of the genus Betula L. in the Czech Republic. J For Sci. 2017;63(12):531–7. doi: 10.17221/105/2017-JFS

50. Suda J, Pyšek P. Flow cytometry in botanical research: introduction. Preslia. 2010;82:1–2.

51. Chung J, Lee J-H, Arumuganathan K, Graef GL, Specht JE. Relationships between nuclear DNA content and seed and leaf size in soybean. Theoretical and Applied Genetics. 1998;96(8):1064–8. doi: 10.1007/s001220050840

52. Otto F. Chapter 11 DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In: Darzynkiewicz Z, Crissman HA, editors. Methods in Cell Biology. 33: Academic Press; 1990. p. 105–10.

53. Greilhuber J, Doležel J, Lysák MA, Bennett MD. The origin, evolution and proposed stabilization of the terms ‘Genome Size’ and ‘C-Value’ to describe nuclear DNA contents. Ann Bot (London). 2005;95(1):255–60. doi: 10.1093/aob/mci019 15596473

54. Sýkora T, Hadač E. Příspěvek k fytogeografii Adršpašsko-Teplických skal [Contribution to the phytogeography of the Adršpach-Teplice rock complex]. Preslia. 1984;56:359–76.

55. Šída O. První přiblížení k problematice bříz (Betula) na Šumavě [The first attempt to solve the Betula taxonomy in the Šumava Mts. Zprávy České botanické společnosti, Praha. 1997;32:187–8.

56. Hejtmánek J. K systematickému hodnocení Betula atrata DOMIN. Preslia. 1956;28:245–9.

57. Baláš M, Kuneš I, Gallo J, Rašáková N. Review on Betula oycoviensis and foliar morphometry of the species in Volyne, Czech Republic. Dendrobiology. 2016;76:117–25. doi: 10.12657/denbio.076.011

58. Franz WR. Die Karpaten Birke, Betula carpatica Waldst. et Kit. [= B. pubescens Ehrh. subsp. carpatica (Waldst. et Kit.) Asch. et Graebner] in Kärnten. Carinthia II. 1995;53(Sonderheft):29–32.

59. Buriánek V, Novotný P, Frýdl J. Metodická příručka k určování domácích druhů bříz [Methodological manual for native birch species determination]. Jíloviště: Výzkumný ústav lesního hospodářství a myslivosti; 2014. 40 p.

60. Missbach R. Betula carpatica Willd., Betula nana L., und ihre Bastare im höchsten Erzgebirge Allgemeine botanische Zeitschrift für Systematik, Floristik, Pflanzengeographie etc. 1908;14:120–3.

61. Ešnerová J, Karlík P, Zahradník D, Koňasová T, Stejskal J, Baláš M, et al. Morfologická variabilita rodu bříza (Betula L.) v Krkonoších se zaměřením na tetraploidní zástupce. [Morphological variability of birch genus (Betula L.) in the Krkonoše Mts with focus on the tetraploid taxa]. Zprávy lesnického výzkumu. 2012;57(2):112–25.

62. Ešnerová J, Vítámvás J, Koňasová T, Kolář F, Baláš M, Karlík P, et al. Využití obrysové analýzy při sledování morfologické variability listů rodu bříza (Betula L.). [Observation of the morphological variability of leaves in Betula L. genus using the quantitative evaluation of outline shapes]. Zprávy lesnického výzkumu. 2013;58(2):107–14.

63. Kulju KKM, Pekkinen M, Varvio S. Twenty-three microsatellite primer pairs for Betula pendula (Betulaceae). Molecular Ecology Notes. 2004;4(3):471–3. doi: 10.1111/j.1471-8286.2004.00704.x

64. Tsuda Y, Ueno S, Ide Y, Tsumura Y. Development of 14 EST-SSRs for Betula maximowicziana and their applicability to related species. Conservation Genetics. 2009;10(3):661–4. doi: 10.1007/s10592-008-9608-z

65. Tsuda Y, Ueno S, Ranta J, Salminen K, Ide Y, Shinohara K, et al. Development of 11 EST-SSRs for Japanese white birch, Betula platyphylla var. japonica and their transferability to related species. Conservation Genetics. 2009;10(5):1385–8. doi: 10.1007/s10592-008-9701-3

66. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–59. 10835412

67. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164(4):1567–87. 12930761

68. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes. 2007;7(4):574–8. doi: 10.1111/j.1471-8286.2007.01758.x 18784791

69. Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Molecular ecology resources. 2009;9(5):1322–32. doi: 10.1111/j.1755-0998.2009.02591.x 21564903

70. Porras-Hurtado L, Ruiz Y, Santos C, Phillips C, Carracedo A, Lareu MV. An overview of STRUCTURE: applications, parameter settings, and supporting software. Frontiers in Genetics. 2013;4:1–13. doi: 10.3389/fgene.2013.00098 23755071.

71. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology. 2005;14(8):2611–20. doi: 10.1111/j.1365-294X.2005.02553.x 15969739

72. Earl DA, vonHoldt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources. 2012;4(2):359–61. doi: 10.1007/s12686-011-9548-7

73. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23(14):1801–6. doi: 10.1093/bioinformatics/btm233 17485429

74. Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes. 2004;4(1):137–8. doi: 10.1046/j.1471-8286.2003.00566.x

75. Bruvo R, Michiels NK, D’Souza TG, Schulenburg H. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Molecular Ecology. 2004;13(7):2101–6. doi: 10.1111/j.1365-294X.2004.02209.x 15189230

76. R_Core_Team. A Language and Environment for Statistical Computing. Viena Austria: R Foundation for Statistical Computing; 2016.

77. Clark LV, Jasieniuk M. Polysat: an R package for polyploid microsatellite analysis. Molecular Ecology Resources. 2011;11(3):562–6. doi: 10.1111/j.1755-0998.2011.02985.x 21481215

78. Hynynen J, Niemstö P, Viherä-Aarnio A, Brunner A, Hein S, Velling P. Silviculture of birch (Betula pendula Roth and Betula pubescens Ehrh.) in northern Europe. Forestry. 2010;83(1):103–19.

79. Greilhuber J, Speta F. Geographical variation of genome size at low taxonomic levels in the Scilla bifolia alliance (Hyacinthaceae). Flora. 1985;176(5):431–8. https://doi.org/10.1016/S0367-2530(17)30139-1.

80. Realini MF, Poggio L, Cámara-Hernández J, González GE. Intra-specific variation in genome size in maize: cytological and phenotypic correlates. AoB PLANTS. 2015;8(plv138):1–12. doi: 10.1093/aobpla/plv138 26644343.

81. Wakamiya I, Newton RJ, Johnston JS, Price HJ. Genome size and environmental factors in the genus Pinus. Am J Bot. 1993;80(11):1235–41. doi: 10.2307/2445706

82. Thórsson ÆT, Pálsson S, Sigurgeirsson A, Anamthawat-Jónsson K. Morphological Variation among Betula nana (diploid), B. pubescens (tetraploid) and their Triploid Hybrids in Iceland. Ann Bot (London). 2007;99(6):1183–93. doi: 10.1093/aob/mcm060 17495985

83. Gill JA, Davy AJ. Variation and polyploidy within lowland populations of the Betula pendula/B. pubescens complex. New Phytol. 1983;94(3):433–51. doi: 10.1111/j.1469-8137.1983.tb03457.x

84. Willdenow KL. Caroli a Linné Species plantarum: exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas: Berolini; 1805. 629 p.

85. Waldstein FdPAGv, Kitaibel P. Descriptiones et icones plantarum rariorum Hungariae. Vol. 1. Viennae (Vienna, Austria): Typis Matthiae Andreae Schmidt; 1802.

86. Waldstein FdPAGv, Kitaibel P. Descriptiones et icones plantarum rariorum Hungariae. Vol. 2. Viennae (Vienna, Austria): Typis Matthiae Andreae Schmidt; 1805.

87. Anonymus. Einige Blumen af das Grab Paul Kitaibel’s /Biographische Notizen/. Flora oder Botanische Zeitung: welche Recensionen, Abhandlungen, Aufsätze, Neuigkeiten und Nachrichten, die Botanik betreffend, enthält. 1831;14(1):149–59.

88. Kirschner J, Kirschnerová L, Štěpánek J. Generally accepted plant names based on material from the Czech Republic and published in 1753–1820. Preslia. 2007;79:323–69.

89. Lamarck J-B. Encyclopédie méthodique. Botanique. Supplement. Paris: Agasse; 1810. 782 p.

90. Presl JS, Presl KB. Flora Čechica: indicatis medicinalibus, oeconomicis technologicisque plantis—Kwětena česká: S poznamenánjm lekařských, hospodařských a řemeselnických rostlin. Prague: Calve, J.G.; 1819. 248 p.

91. Lejeune ALS, Courtois RJ. Compendium florae Belgicae. Conjunctis studiis ediderunt Lejeune A. L. S. & Courtois R.: Leodii,Apud P. J. Collardin; 1836. 292 p.

92. Reichenbach HGL, Reichenbach HG. Icones florae Germanicae et Helveticae, simul Pedemontanae, Tirolensis, Istriacae, Dalmaticae, Austriacae, Hungaricae, Transylvanicae, Moravicae, Borussicae, Holsaticae, Belgicae, Hollandicae, ergo Mediae Europae. 2nd ed. Leipsic, Germany: F. Hofmeister [etc.]; 1850. 338 p.

93. Wimmer F. Bericht der botanischen Section im Jahre 1838. In: Wendt J, editor. Uebersicht der Arbeiten und Veränderungen der der Schlesischen Gesellschaft für Vaterländische Cultur im Jahre 1838. Breslau: Grass, Barth und Comp.; 1839. p. 123–38.

94. Willkomm HM. Forstliche Flora von Deutschland und Oesterreich; oder, Forstbotanische und pflanzengeographische Beschreibung aller im Deutschen Reich und Oesterreichischen Kaiserstaat heimischen und im Freien angebauten oder anbauungswürdigen Holzgewächse. 2. vielfach verm., verb. und wesentlich veränd. Auflage ed. Leipzig, Germany: Winter, C.F.; 1887. 968 p.

95. Morgenthaler H. Beiträge zur Kenntnis des Formenkreises der Sammelart Betula alba L. mit variationsstatistischer Analyse der Phaenotypen. Vierteljahresschr Naturforsch Ges Zürich. 1915;60:433–567.

96. McNeill J. Holotype specimens and type citations: General issues. Taxon. 2014;63(5):1112–3. doi: 10.12705/635.7

97. Steenis CGGJV. Specific and infraspecific delimitation. Flora Malesiana, Series 1. 1957;5(1):167–234.

98. Olšavská K. Betula L. In: Goliašová K, Michalková E, editors. Flóra Slovenska V/3. Bratislava, Slovak Republic: VEDA, vydavateľstvo Slovenskej akadémie vied 2006. p. 144–67.

99. Kaplan Z, editor. Klíč ke květeně České republiky [Key to the flora of the Czech Republic; revised and updated edition]. Praha, Czech Republic: Academia; 2019.

100. Thórsson ÆT, Pálsson S, Lascoux M, Anamthawat-Jónsson K. Introgression and phylogeography of Betula nana (diploid), B. pubescens (tetraploid) and their triploid hybrids in Iceland inferred from cpDNA haplotype variation. Journal of Biogeography. 2010;37(11):2098–110. doi: 10.1111/j.1365-2699.2010.02353.x

101. Chytrý M, Danihelka J, Kaplan Z, Pyšek P. Flora and Vegetation of the Czech Republic. Cham (Switzerland): Springer; 2017. 466 p.

102. Petr L, Novák J. High vegetation and environmental diversity during the Late Glacial and Early Holocene on the example of lowlands in the Czech Republic. Biologia. 2014;69(7):847–62. doi: 10.2478/s11756-014-0381-9

103. Kuneš P, Pelánková B, Chytrý M, Jankovská V, Pokorný P, Petr L. Interpretation of the last-glacial vegetation of eastern-central Europe using modern analogues from southern Siberia. Journal of Biogeography. 2008;35(12):2223–36. doi: 10.1111/j.1365-2699.2008.01974.x

104. Mallet J. Subspecies, Semispecies, Superspecies: Elsevier; 2007.

105. Zachos FE. Species Concepts in Biology: Historical Development, Theoretical Foundations and Practical Relevance. 1 ed: Springer International Publishing; 2016. XII, 220 p.


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