Abstract
The Balkan Peninsula is widely acknowledged as one of the centers of European biodiversity and a major glacial refugium for plant species. Its extensive geographic heterogeneity and diverse mosaic of habitats, coupled with relatively high environmental stability over long periods, have enabled the diversification of lineages and simultaneously fostered the long-term survival of diverse species. The increasing number of phylogeographically studied plant species in the region has substantially contributed to a better understanding of the relationships among closely related taxa and provided significant insights into intraspecific lineage differentiation. The present paper reviews the current knowledge on plant phylogeography in the Balkan Peninsula. By providing an updated overview of the most recent studies dealing with the diversity and evolution of Balkan plants, we explore the phylogeographic patterns and roles of refugia in structuring genetic diversity and highlight the crucial evolutionary processes that shaped the diversity of plants in the region. Molecular clock-based estimations highlight the importance of Pleistocene climatic fluctuations across taxonomic groups and lineage distribution patterns corroborate the persistence of multiple glacial refugia. Spatial congruence in phylogeographic splits is determined and discussed. An examination of phylogeographic connections with adjacent regions (i.e., the Alps, Apennine Peninsula, Asia Minor, Carpathians, and central Europe) uncovers several consistent patterns. Additionally, allopatric and ecological speciation, polyploidy, and hybridization are identified as crucial evolutionary mechanisms acting in the Balkan Peninsula and shaping species diversity. Furthermore, the existing research gaps are identified and future approaches with the potential to better understand the unique Balkan flora are highlighted.
Similar content being viewed by others
References
Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Möst M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D (2013) Hybridization and speciation. J Evol Biol 26:229–246. https://doi.org/10.1111/j.1420-9101.2012.02599.x
Abbott RJ, Rieseberg LH (2012) Hybrid Speciation. Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0001753.pub2
Ali T, Muñoz-Fuentes V, Buch AK, Çelik A, Dutbayev A, Gabrielyan I, Glynou K, Kachour L, Khaliq I, Kitner M, Nigrelli L, Plocha S, Runge F, Solovyeva I, Schmuker A, Vakhrusheva L, Xia X, Maciá-Vicente JG, Nowak C, Thinesa M (2019) Out of Transcaucasica: origin of western and central Palearctic populations of Microthlaspi perfoliatum. Flora 253:127–141. https://doi.org/10.1016/j.flora.2019.02.012
Ali T, Runge F, Dutbayev A, Schmuker A, Solovyeva I, Nigrelli L, Buch AK, Xia X, Ploch S, Orren O, Kummer V, Paule J, Ҫelik A, Vakhrusheva L, Gabrielyan I, Thines M (2016) Microthlaspi erraticum (Jord.) T. Ali et Thines has a wide distribution, ranging from the Alps to the Tien Shan. Flora 225:76–81. https://doi.org/10.1016/j.flora.2016.09.008
Ansell SW, Stenøien HK, Grundmann M, Russell SJ, Koch MA, Schneider H, Vogel JC (2011) The importance of Anatolian mountains as the cradle of global diversity in Arabis alpina, a key arctic–alpine species. Ann Bot (Oxford) 108:241–252. https://doi.org/10.1093/aob/mcr134
Arrigo N, de La Harpe M, Litsios G, Zozomová-Lihová J, Španiel S, Marhold K, Barker MS, Alvarez N (2016) Is hybridization driving the evolution of climatic niche in Alyssum montanum? Amer J Bot 103:1348–1357. https://doi.org/10.3732/ajb.1500368
Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Rev Ecol Syst 18:489–522. https://doi.org/10.1146/annurev.es.18.110187.002421
Bardy KE, Albach DC, Schneeweiss GM, Fischer MA, Schönswetter P (2010) Disentangling phylogeography, polyploid evolution and taxonomy of a woodland herb (Veronica chamaedrys group, Plantaginaceae s.l.) in southeastern Europe. Molec Phylogen Evol 57:771–786. https://doi.org/10.1016/j.ympev.2010.06.025
Bardy KE, Schönswetter P, Schneeweiss GM, Fischer MA, Albach DC (2011) Extensive gene flow blurs species boundaries among Veronica barrelieri, V. orchidea and V. spicata (Plantaginaceae) in southeastern Europe. Taxon 60:108–121. https://doi.org/10.1002/tax.601010
Bareka P, Siljak-Yakovlev S, Kamari G (2012) Molecular cytogenetics of Bellevalia (Hyacinthaceae) species occurring in Greece. Pl Syst Evol 298:421–430. https://doi.org/10.1007/s00606-011-0555-7
Barker BS, Andonian K, Swope SM, Luster DG, Dlugosch KM (2017) Population genomic analyses reveal a history of range expansion and trait evolution across the native and invaded range of yellow starthistle (Centaurea solstitialis). Molec Ecol 26:1131–1147. https://doi.org/10.1111/mec.13998
Barker MS, Arrigo N, Baniaga AE, Li Z, Levin DA (2016) On the relative abundance of autopolyploids and allopolyploids. New Phytol 210:391–398. https://doi.org/10.1111/nph.13698
Bernardo L, Maiorca G, Roma-Marzio F, Peruzzi L (2018) Alyssum doerfleri Degen (Brassicaceae), new for the Italian flora. Phytotaxa 334:10–18. https://doi.org/10.11646/phytotaxa.334.1.2
Bianco P, Medagli P, D’Emerico S, Ruggiero L (1988) Ephedra campylopoda C.A.Meyer (Gnetopsida), nuova per la Flora Italiana. Webbia 42:161–166. https://doi.org/10.1080/00837792.1988.10670434
Bilgin R (2011) Back to the suture: the distribution of intraspecific genetic diversity in and around Anatolia. Int J Molec Sci 12:4080–4103. https://doi.org/10.3390/ijms12064080
Bittkau C, Comes HP (2005) Evolutionary processes in a continental island system: molecular phylogeography of the Aegean Nigella arvensis alliance (Ranunculaceae) inferred from chloroplast DNA. Molec Ecol 14:4065–4083. https://doi.org/10.1111/j.1365-294X.2005.02725.x
Bogdanović S, Ljubičić I, Clementi M (2015) Aegilops uniaristata Vis. (Poaceae): typification and occurrence in Croatia. Acta Bot Croat 74:165–172. https://doi.org/10.1515/botcro-2015-0006
Bognar A, Faivre S, Pavelić J (1991) Glaciation traces on the Northern Velebit. Geogr Glasn 53:27–39
Bognar A, Prugovečki I (1997) Glaciation traces in the area of Risnjak Mountain Massif. Geol Croat 50:269–278
Boyer SL, Karaman I, Giribet G (2005) The genus Cyphophthalmus (Arachnida, Opiliones, Cyphophthalmi) in Europe: a phylogenetic approach to Balkan Peninsula biogeography. Molec Phylogen Evol 36:554–567. https://doi.org/10.1016/j.ympev.2005.04.004
Brullo S, Brullo C, Cambria S, Giusso del Galdo G, Minissale P, Salmeri C, Beccarisi L, Veronico G, Tomaselli V (2019) Poa jubata (Poaceae) a rare Balkan species, first record for Italian flora. Acta Bot Croat 78:147–154. https://doi.org/10.2478/botcro-2019-0020
Buerkle CA, Wolf DE, Rieseberg LH (2003) The origin and extinction of species through hybridization. In: Brigham CA, Schwartz MW (eds) Population viability in plants: conservation, management, and modelling of rare plants. Springer Verlag, Heidelberg, pp 117–141
Buono D, Khan G, von Hagen KB, Kosachev PA, Mayland-Quellhorst E, Mosyakin SL, Albach DC (2021) Comparative Phylogeography of Veronica spicata and V. longifolia (Plantaginaceae) Across Europe: Integrating Hybridization and Polyploidy in Phylogeography. Frontiers Pl Sci 11:588354. https://doi.org/10.3389/fpls.2020.588354
Bureš P, Šmerda J, Michálková E, Šmarda P, Knoll A, Vavrinec M (2018) Cirsium greimleri: a new species of thistle endemic to the eastern Alps and Dinarides. Preslia 90:105–134. https://doi.org/10.2855/preslia.2018.105
Buzurović U, Tomović G, Niketić M, Bogdanović S, Aleksić JM (2020) Phylogeographic and taxonomic considerations on Goniolimon tataricum (Plumbaginaceae) and its relatives from south-eastern Europe and the Apennine Peninsula. Pl Syst Evol 306:29. https://doi.org/10.1007/s00606-020-01636-0
Caković D, Cresti L, Stešević D, Schönswetter P, Frajman B (2021) High genetic and morphological diversification of the Euphorbia verrucosa alliance (Euphorbiaceae) in the Balkan and Iberian peninsulas. Taxon 70:286–307. https://doi.org/10.1002/tax.12427
Caković D, Frajman B (2020) Three Tertiary Euphorbia species persisted in the forests of the Balkan Peninsula. Pl Syst Evol 306:50. https://doi.org/10.1007/s00606-020-01672-w
Caković D, Stešević D, Schönswetter P, Frajman B (2015) How many taxa? Spatiotemporal evolution and taxonomy of Amphoricarpos (Asteraceae, Carduoideae) on the Balkan Peninsula. Org Diversity Evol 15:429–445. https://doi.org/10.1007/s13127-015-0218-6
Carnicero P, Garcia-Jacas N, Sáez L, Constantinidis T, Galbany-Casals M (2021) Disentangling relationships among eastern Mediterranean Cymbalaria including description of a novel species from the southern Peloponnese (Greece). Pl Syst Evol 307:13. https://doi.org/10.1007/s00606-020-01730-3
Carnicero P, Sáez L, Garcia-Jacas N, Galbany-Casals M (2017) Different speciation types meet in a Mediterranean genus: the biogeographic history of Cymbalaria (Plantaginaceae). Taxon 66:393–407. https://doi.org/10.12705/662.7
Castroviejo S, Aldasoro JJ, Alarcón M (2010) Campanulaceae. In: Euro+Med Plantbase—the information resource for Euro-Mediterranean plant diversity. http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Cecchi L (2011) A reappraisal of Phyllolepidum (Brassicaceae), a neglected genus of the European flora, and its relationships in tribe Alysseae. Pl Biosyst 145:818–831. https://doi.org/10.1080/11263504.2011.580789
Cecchi L, Španiel S, Bianchi E, Coppi A, Gonnelli C, Selvi F (2020) Odontarrhena stridii (Brassicaceae), a new nickel-hyperaccumulating species from mainland Greece. Pl Syst Evol 306:69. https://doi.org/10.1007/s00606-020-01687-3
Cetlová V, Zozomová-Lihová J, Mártonfiová L, Melichárková A, Španiel S (2021) Multiple drivers of high species diversity and endemism among Alyssum annuals in the Mediterranean: the evolutionary significance of the Aegean hotspot. Frontiers Pl Sci 12:627909. https://doi.org/10.3389/fpls.2021.627909
Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482. https://doi.org/10.1038/nrg3503
Cieślak E, Drobniak S (2019) Phylogeography of xerothermic Carlina acanthifolia subsp. utzka in Central Europe. Flora 253:76–86. https://doi.org/10.1016/j.flora.2019.03.006
Conti F, Reich D, Gutermann W (2020) Notes on the genus Echinops L. (Asteraceae) in SE Europe. Adansonia 42:95–104. https://doi.org/10.5252/adansonia2020v42a3
Correggiari A, Roveri M, Trincardi F (1996) Late Pleistocene and Holocene evolution of the North Adriatic Sea. Il Quaternario 9:697–704
Cresti L, Schönswetter P, Peruzzi L, Barfuss MHJ, Frajman B (2019) Pleistocene survival in three Mediterranean refugia: origin and diversification of the Italian endemic Euphorbia gasparrinii from the E. verrucosa alliance (Euphorbiaceae). Bot J Linn Soc 189:262–280. https://doi.org/10.1093/botlinnean/boy082
Cronberg N (2000) Genotypic diversity of the epiphytic bryophyte Leucodon sciudoides in formerly glaciated versus nonglaciated parts of Europe. Heredity 84:710–720. https://doi.org/10.1046/j.1365-2540.2000.00719.x
Crowl AA, Myers C, Cellinese N (2017) Embracing discordance: phylogenomic analyses provide evidence for allopolyploidy leading to cryptic diversity in a Mediterranean Campanula (Campanulaceae) clade. Evolution 71:913–922. https://doi.org/10.1111/evo.13203
Crowl AA, Visger CJ, Mansion G, Hand R, Wu H-H, Kamari G, Phitos D, Cellinese N (2015) Evolution and biogeography of the endemic Roucela complex (Campanulaceae: Campanula) in the Eastern Mediterranean. Ecol Evol 5:5329–5343. https://doi.org/10.1002/ece3.1791
Daneck H, Fér T, Marhold K (2016) Glacial survival in northern refugia? Phylogeography of the temperate shrub Rosa pendulina L. (Rosaceae): AFLP vs. chloroplast DNA variation. Biol J Linn Soc 119:704–718. https://doi.org/10.1111/bij.12619
Dimopoulos P, Raus T, Bergmeier E, Constantinidis T, Iatrou G, Kokkini S, Strid A, Tzanoudakis D (2013) Vascular plants of Greece: an annotated checklist. Englera 31:1–372
Di Pietro R, D’Amato G, Trombetta B (2005) Karyology and distribution of Sesleria tenuifolia complex (Poaceae) in the Italian Peninsula. Nordic J Bot 23:615–623. https://doi.org/10.1111/j.1756-1051.2003.tb00442.x
Di Pietro R, Wagensommer R (2014) A new Sesleria juncifolia association from the south-eastern Italy and its position in the amphi-Adriatic biogeographical context. Acta Bot Croat 73:171–207. https://doi.org/10.2478/botcro-2013-0018
Domínguez Lozano F, Galicia Herbada D, Moreno Rivero L, Moreno Saiz JC, Sainz Ollero H (2000) Areas of high floristic endemism in Iberia and the Balearic Islands: an approach to biodiversity conservation using narrow endemics. Belgian J Entomol 2:171–185
Duffy KJ, Jacquemyn H (2019) Climate change increases ecogeographical isolation between closely related plants. J Ecol 107:167–177. https://doi.org/10.1111/1365-2745.13032
Đurović S, Schönswetter P, Niketić M, Tomović G, Frajman B (2017) Disentangling relationships among the members of the Silene saxifraga alliance (Caryophyllaceae): phylogenetic structure is geographically rather than taxonomically segregated. Taxon 66:343–364. https://doi.org/10.1705/662.4
Đurović SZ, Temunović M, Niketić M, Tomović G, Schönswetter P, Frajman B (2021) Impact of Quaternary climatic oscillations on phylogeographic patterns of three habitat-segregated Cerastium taxa endemic to the Dinaric Alps. J Biogeogr 48:2022–2036. https://doi.org/10.1111/jbi.14133
Essl F, Staudinger M, Stöhrc O, Schratt-Ehrendorferd L, Rabitsch W, Niklfeld H (2009) Distribution patterns, range size and niche breadth of Austrian endemic plants. Biol Conservation 142:2547–2558. https://doi.org/10.1016/j.biocon.2009.05.027
Falch M, Schönswetter P, Frajman B (2019) Both vicariance and dispersal have shaped the genetic structure of Eastern Mediterranean Euphorbia myrsinites (Euphorbiaceae). Perspect Pl Ecol Evol Syst 39:125459. https://doi.org/10.1016/j.ppees.2019.125459
Fanelli G, Attorre F, Del Giudice M, Gjeta E, De Sanctis M (2015) Phlomis fruticosa scrublands in the central Medi-terranean region: syntaxonomy and ecology. Phytocoenologia 45:49–68. https://doi.org/10.1127/phyto/2015/0041
Fassou G, Kougioumoutzis K, Iatrou G, Trigas P, Papasotiropoulos V (2021) Genetic diversity and range dynamics of Helleborus odorus subsp. cyclophyllus under different climate change scenarios. Forests 11:620. https://doi.org/10.3390/f11060620
Favre LF, Fluteau F, Cheddadi R, Thévenod L, Suc JP (2007) Messinian vegetation maps of the Mediterranean region using models and interpolated pollen data. Geobios (Lyon) 40:433–443. https://doi.org/10.1016/j.geobios.2006.12.002
Frajman B, Eggens F, Oxelman B (2009) Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae)—a multigene phylogenetic approach with relative dating. Syst Biol 58:328–345. https://doi.org/10.1093/sysbio/syp030
Frajman B, Oxelman B (2007) Reticulate phylogenetics and phytogeographical structure of Heliosperma (Sileneae, Caryophyllaceae) inferred from chloroplast and nuclear DNA sequences. Molec Phylogen Evol 43:140–155. https://doi.org/10.1016/j.ympev.2006.11.003
Frajman B, Rešetnik I, Niketić M, Ehrendorfer F, Schönswetter P (2016) Patterns of rapid diversification in heteroploid Knautia sect. Trichera (Caprifoliaceae, Dipsacoideae), one of the most intricate taxa of the European flora. BMC Evol Biol 16:204–204. https://doi.org/10.1186/s12862-016-0773-2
Frajman B, Schneeweiss GM (2009) A campanulaceous fate: the Albanian stenoendemic Asyneuma comosiforme in fact belongs to isophyllous Campanula. Syst Bot 34:595–601. https://doi.org/10.1600/03636440978927117
Frajman B, Schönswetter P (2017) Amphi-Adriatic distributions in plants revisited: Pleistocene trans-Adriatic dispersal in the Euphorbia barrelieri group (Euphorbiaceae). Bot J Linn Soc 185:240–252. https://doi.org/10.1093/botlinnean/box055
Frajman B, Záveská E, Gamisch A, Moser T, The STEPPE Consortium, Schönswetter P (2019) Integrating phylogenomics, phylogenetics, morphometrics, relative genome size and ecological niche modelling disentangles the diversification of Eurasian Euphorbia seguieriana s. l. (Euphorbiaceae). Molec Phylogen Evol 134:238–252. https://doi.org/10.1016/j.ympev.2018.10.046
Garcia-Jacas N, López-Pujol J, López-Vinyallonga S, Janaćković P, Susanna A (2019) Centaurea subsect. Phalolepis in Southern Italy: ongoing speciation or species overestimation? Genetic evidence based on SSRs analyses. Syst Biodivers 17:93–109. https://doi.org/10.1080/14772000.2018.1549617
Georghiou K, Delipetrou P (2010) Patterns and traits of the endemic plants of Greece. Bot J Linn Soc 162:130–422. https://doi.org/10.1111/j.1095-8339.2010.01025.x
Glasnović P, Temunović M, Lakušić D, Rakić T, Brečko Grubar V, Surina B (2018) Understanding biogeographical patterns in the western Balkan Peninsula using environmental niche modelling and geostatistics in polymorphic Edraianthus tenuifolius. AoB Plants 10:ply064. https://doi.org/10.1093/aobpla/ply064
Gómez A, Lunt DH (2007) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N (eds) Phylogeography of Southern European refugia. Springer, Berlin, pp 155–188. https://doi.org/10.1007/1-4020-4904-8
Gömöry D, Zhelev P, Brus R (2020) The Balkans: a genetic hotspot but not a universal colonization source for trees. Pl Syst Evol 306:5. https://doi.org/10.1007/s00606-020-01647-x
Gottschlich G, Domina G, Di Gristina E (2017) Hieracium umbrosum subsp. abietinum (Asteraceae), a further example of amphi-Adriatic disjunction. Pl Biosyst 151:792–794. https://doi.org/10.1080/11263504.2017.1341439
Grdiša M, Liber Z, Radosavljević I, Carović-Stanko K, Kolak I, Satovic Z (2014) Genetic diversity and structure of Dalmatian Pyrethrum (Tanacetum cinerariifolium Trevir. /Sch./ Bip., Asteraceae) within the Balkan Refugium. PLoS ONE 9:e105265. https://doi.org/10.1371/journal.pone.0105265
Grdiša M, Radosavljević I, Liber Z, Stefkov G, Ralli P, Chatzopoulou PS, Carović-Stanko K, Šatović Z (2019) Divergent selection and genetic structure of Sideritis scardica populations from southern Balkan Peninsula as revealed by AFLP fingerprinting. Sci Rep 9:12767. https://doi.org/10.1038/s41598-019-49097-x
Greuter W (1979) The origins and evolution of island floras as exemplified by the Aegean Archipelago. In: Bramwell D (ed) Plants and Islands. Academic Press, London, New York, pp 87–106
Greuter W (2006 onwards) Compositae (pro parte majore). In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Grundmann M, Ansell SW, Russell SJ, Koch MA, Vogel JC (2008) Hotspots of diversity in a clonal world—the Mediterranean moss Pleurochaete squarrosa in Central Europe. Molec Ecol 17:825–838. https://doi.org/10.1111/j.1365-294X.2007.03634.x
Hammoud C, Kougioumoutzis K, Rijsdijk KF, Simaiakis SM, Norder SJ, Foufopoulos J, Georgopoulou E, Loon EE (2021) Past connections with the mainland structure patterns of insular species richness in a continental-shelf archipelago (Aegean Sea, Greece). Ecol Evol 11:5441–5458. https://doi.org/10.1002/ece3.7438
Hand R (2011) Apiaceae. In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Hardion L, Baumel A, Verlaque R, Vila B (2014) Distinct evolutionary histories of lowland biota on Italian and Balkan peninsulas revealed by the phylogeography of Arundo plinii (Poaceae). J Biogeogr 41:2150–2161. https://doi.org/10.1111/jbi.12355
Hardion L, Dumas PJ, Abdel-Samad F, Dager Kharrat MB, Surina B, Affre L, Médail F, Bacchetta G, Baumel A (2016) Geographical isolation caused the diversification of the Mediterranean thorny cushion-like Astragalus L. sect. Tragacantha DC. (Fabaceae). Molec Phylogen Evol 97:187–195. https://doi.org/10.1016/j.ympev.2016.01.006
Harlan JR, De Wet JMJ (1975) On Ö. Winge and a prayer: the origins of polyploidy. Bot Rev 41:361–390. https://doi.org/10.1007/BF02860830
Hedderson TA, Nowell TL (2006) Phylogeography of Homalothecium sericeum (Hedw.) Br. Eur.; toward a reconstruction of glacial survival and postglacial migration. J Bryol 28:283–292. https://doi.org/10.1179/174328206X136287
Hellwig FH (2004) Centaureinae (Asteraceae) in the Mediterranean – history of ecogeographical radiation. Pl Syst Evol 246:137–162. https://doi.org/10.1007/s00606-004-0150-2
Hewitt MG (1999) Post-glacial re-colonisation of European biota. Biol J Linn Soc 68:87–112. https://doi.org/10.1006/bijl.1999.0332
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. https://doi.org/10.1038/35016000
Hewitt GM (2011) Mediterranean peninsulas: the evolution of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer, Berlin, pp 123–147. https://doi.org/10.1007/978-3-642-20992-5
Hodálová I, Mártonfiová L, Skokanová K, Majerová M, Somlyay L, Mereďa P (2020) The utility of genome size in plant identification: a case study on Sesleria (Poaceae) from Croatia and Slovenia. Pl Syst Evol 306:87. https://doi.org/10.1007/s00606-020-01715-2
Hodková E, Doudová J, Douda J, Krak K, Mandák B (2019) On the road: Postglacial history and recent expansion of the annual Atriplex tatarica in Europe. J Biogeogr 46:2609–2621. https://doi.org/10.1111/jbi.13687
Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485. https://doi.org/10.1038/nature09670
Hopkins R (2013) Reinforcement in plants. New Phytol 197:1095–1103. https://doi.org/10.1111/nph.12119
Hörandl E, Raab-Straube E (2015) Ranuculaceae. In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Horvat I, Glavač V, Ellenberg H (1974) Vegetation Südosteuropas. Fischer, Stuttgart
Hsü KJ, Montadert L, Bernoulli D, Cita MB, Erickson A, Garrison RE, Kidd RB, Mélières F, Müller C, Wright R (1977) History of the Mediterranean salinity crisis. Nature 267:399–403. https://www.nature.com/articles/267399a0
Ilyinska A, Ryff L, Yevseyenkov P, Svirin S (2021) Alyssum smyrnaeum (Brassicaceae): new records for the Crimean flora. Phytol Balcan 27:59–69
Ivanov D, Utescher T, Mosbrugger V, Syabryaj S, Djordjević-Milutinović D, Molchanoff S (2011) Miocene vegetation and climate dynamics in eastern and central Paratethys (southeastern Europe). Palaeogeogr Palaeoclimatol Palaeoecol 304:262–275. https://doi.org/10.1016/j.palaeo.2010.07.006
Janković I, Satovic Z, Liber Z, Kuzmanović N, Di Pietro R, Radosavljević I, Nikolov Z, Lakušić D (2019) Genetic and morphological data reveal new insights into the taxonomy of Campanula versicolor s.l. (Campanulaceae). Taxon 68:340–369. https://doi.org/10.1002/tax.12050
Janković I, Šatović Z, Liber Z, Kuzmanović N, Radosavljević I, Lakušić D (2016) Genetic diversity and morphological variability in the Balkan endemic Campanula secundiflora s.l. (Campanulaceae). Bot J Linn Soc 180:64–88. https://doi.org/10.1111/boj.12359
Jaros U, Tribsch A, Comes HP (2018) Diversification in continental island archipelagos: new evidence on the roles of fragmentation, colonizcolonisation and gene flow on the genetic divergence of Aegean Nigella (Ranunculaceae). Ann Bot (Oxford) 121:241–254. https://doi.org/10.1093/aob/mcx150
Jug-Dujaković M, Ninčević T, Liber Z, Grdiša M, Šatović Z (2020) Salvia officinalis survived in situ Pleistocene glaciation in ‘refugia within refugia’ as inferred from AFLP markers. Pl Syst Evol 306:38. https://doi.org/10.1007/s00606-020-01665-9
Kabaš E, Niketić M, Ćušterevska R, Tomović G, Vukojičić S, Lakušić D (2019) Stipa crassiculmis subsp. picentina (Poaceae) new for the Balkans – a further example of amphi-Adriatic disjunction. Pl Biosyst 153:32–38. https://doi.org/10.1080/11263504.2018.1436612
Karbstein K, Tomasello S, Hodač L, Dunkel FG, Daubert M, Hörandl E (2020) Phylogenomics supported by geometric morphometrics reveals delimitation of sexual species within the polyploid apomictic Ranunculus auricomus complex (Ranunculaceae). Taxon 69:1191–1220. https://doi.org/10.1002/tax.12365
Karl R, Scholz H (2009) Bromus parvispiculatus H. Scholz. In: Greuter W, Raus T (eds) Med-Checklist Notulae 28. Willdenowia 39:340
Kiedrzyński M, Zielińska KM, Jedrzejczyk KE, Tomczyk PP, Rewicz A, Rewers M, Indreica A, Bednarska I, Stupar V, Roleček J, Šmarda P (2021) Tetraploids expanded beyond the mountain niche of their diploid ancestors in the mixed-ploidy grass Festuca amethystina L. Sci Rep 11:18735. https://doi.org/10.1038/s41598-021-97767-6
Kolář F, Fuxová G, Záveská E, Nagano AJ, Hyklová L, Lučanová M, Kudoh H, Marhold K (2016) Northern glacial refugia and altitudinal niche divergence shape genome-wide differentiation in the emerging plant model Arabidopsis arenosa. Molec Ecol 25:3929–3949. https://doi.org/10.1111/mec.13721
Kolarčik V, Zozomová-Lihová J, Mártonfi P (2010) Systematics and evolutionary history of the Asterotricha group of the genus Onosma (Boraginaceae) in central and southern Europe inferred from AFLP and nrDNA ITS data. Pl Syst Evol 290:21–45. https://doi.org/10.1007/s00606-010-0346-6
Körner C, Hiltbrunner E (2021) Why is the alpine flora comparatively robust against climatic warming? Diversity 13:383. https://doi.org/10.3390/d13080383
Kosonen Z, Schnyder E, Hiltbrunner E, Thimonier A, Schmitt M, Seitler E, Thöni L (2019) Current atmospheric nitrogen deposition still exceeds critical loads for sensitive, semi-natural ecosystems in Switzerland. Atmos Environ 211:214–225. https://doi.org/10.1016/j.atmosenv.2019.05.005
Kougioumoutzis K, Kokkoris IP, Panitsa M, Kallimanis A, Strid A, Dimopoulos P (2021) Plant endemism centres and biodiversity hotspots in Greece. Biology 10:72. https://doi.org/10.3390/biology10020072
Kougioumoutzis K, Valli AT, Georgopoulou E, Simaiakis SM, Triantis KA, Trigas P (2017) Network biogeography of a complex island system: The Aegean Archipelago revisited. J Biogeogr 44:651–660. https://doi.org/10.1111/jbi.12920
Kramp K, Huck S, Niketić M, Tomović G, Schmitt T (2009) Multiple glacial refugia and complex postglacial range shifts of the obligatory woodland plant species Polygonatum verticillatum (Convallariaceae). Pl Biol 11:392–404. https://doi.org/10.1111/j.1438-8677.2008.00130.x
Krijgsman W (2002) The Mediterranean: mare nostrum of earth sciences. Earth Planet Sci Lett 205:1–12. https://doi.org/10.1016/S0012-821X(02)01008-7
Krijgsman W, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400:652–655. https://www.nature.com/articles/23231
Kropf M, Kadereit JW, Comes HP (2003) Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Molec Ecol 12:931–949. https://doi.org/10.1046/j.1365-294X.2003.01781.x
Krstić N, Savić L, Jovanović G (2012) The Neogene lakes on the Balkan land. Geol Anali Balkan Poluostrva 73:37–60. https://doi.org/10.2298/GABP1273037K
Kryštufek B, Reed JM (2004) Pattern and processes in Balkan biodiversity—an overview. In: Griffits HI, Kryštufek B, Reed JM (eds) Balkan biodiversity, pattern and process in the European hotspot. Kluwer, Dordrecht, pp 203–217
Kučera J, Marhold K, Lihová J (2010) Cardamine maritima group (Brassicaceae) in the amphi-Adriatic area: a hotspot of species diversity revealed by DNA sequences and morphological variation. Taxon 59:148–164. https://www.jstor.org/stable/27757059
Kučera J, Tremetsberger K, Vojta J, Marhold K (2008) Molecular study of the Cardamine maritima group (Brassicaceae) from Balkan and Apennine Peninsulas based on amplified fragment length polymorphism (AFLP). Pl Syst Evol 275:193–207. https://doi.org/10.1007/s00606-008-0061-8
Kukla GJ, Bender ML, de Beaulieu J-L, Bond G, Broecker WS, Cleveringa P, Gavin JE, Herbert TD, Imbrie J, Jouzel J, Keigwin LD, Knudsen K-L, McManus JF, Merkt J, Muhs DR, Muller H, Poore RZ, Porter SC, Seret G, Schackleton NJ, Turner C, Tzdedakis PC, Winograd IJ (2002) Last Interglacial Climates. Quatern Res 58:2–13. https://doi.org/10.1006/qres.2001.2316
Kutnjak D, Schönswetter P, Dullinger S, Kuttner M, Niketić M, Frajman B (2014) Escaping to the summits: phylogeography and predicted range dynamics of Cerastium dinaricum, an endangered high mountain plant endemic to the western Balkan Peninsula. Molec Phylogen Evol 78:365–374. https://doi.org/10.1016/j.ympev.2014.05.015
Kuzmanović N, Comanescu P, Frajman B, Lazarević M, Paun O, Schönswetter P, Lakušić D (2013) Genetic, cytological and morphological differentiation within the Balkan-Carpathian Sesleria rigida sensu Fl. Eur. (Poaceae): A taxonomically intricate tetraploid-octoploid complex. Taxon 62:458–472. https://doi.org/10.12705/623.13
Kuzmanović N, Lakušić D, Frajman B, Alegro A, Schönswetter P (2017) Phylogenetic relationships in Seslerieae (Poaceae) including resurrection of Psilathera and Sesleriella, two monotypic genera endemic to the Alps. Taxon 66:1349–1370
Kuzmanović N, Lakušić D, Frajman B, Stevanoski I, Conti F, Schönswetter P (2021) Long neglected diversity in the Accursed Mountains (western Balkan Peninsula): Ranunculus bertisceus is a genetically and morphologically divergent new species. Bot J Linn Soc 196:384–406. https://doi.org/10.1093/botlinnean/boab001
Kyrkjeeide MO, Hassel K, Flatberg KI, Stenøien HK (2012) The rare peat moss Sphagnum wulfianum (Sphagnaceae) did not survive the last glacial period in northern European refugia. Amer J Bot 99:677–689. https://doi.org/10.3732/ajb.1100410
Kyrkjeeide MO, Stenøien HK, Flatberg KI, Hassel K (2014) Glacial refugia and post-glacial colonization patterns in European bryophytes. Lindbergia 37:47–59. https://www.jstor.org/stable/lindbergia.37.47
Kyrkou I, Iriondo JM, García-Fernández A (2015) A glacial survivor of the alpine Mediterranean region: phylogenetic and phylogeographic insights into Silene ciliata Pourr. (Caryophyllaceae). PeerJ 3:e1193. https://doi.org/10.7717/peerj.1193
Lack HW, Barina Z (2002) The early botanical exploration of Albania (1839–1945). Willdenowia 50:519–558. https://doi.org/10.3372/wi.50.50304
Lakušić D, Liber Z, Nikolić T, Surina B, Kovačić S, Bogdanović S, Stefanović S (2013) Molecular phylogeny of the Campanula pyramidalis species complex (Campanulaceae) inferred from chloroplast and nuclear non-coding sequences and its taxonomic implications. Taxon 62:505–524. https://doi.org/10.12705/623.1
Lakušić D, Rakić T, Stefanović S, Surina B, Stevanović V (2009) Edraianthus × lakusicii (Campanulaceae), a new intersectional natural hybrid: morphological and molecular evidence. Pl Syst Evol 280:77–88. https://doi.org/10.1007/s00606-009-0168-6
Larridon I, Villaverde T, Zuntini AR, Pokorny L, Brewer GE, Epitawalage N, Fairlie I, Hahn M, Kim J, Maguilla E, Maurin O, Xanthos M, Hipp AL, Forest F, Baker WJ (2020) Tackling rapid radiations with targeted sequencing. Frontiers Pl Sci 10:1655. https://doi.org/10.3389/fpls.2019.01655
Laskaris N, Sampson A, Mavridis F, Liritzis I (2011) Late Pleistocene/Early Holocene seafaring in the Aegean: new obsidian hydration dates with the SIMS-SS method. J Archaeol Sci 38:2475–2479. https://doi.org/10.1016/j.jas.2011.05.019
Lazarević M, Kuzmanović N, Lakušić D, Alegro A, Schönswetter P, Frajman B (2015) Patterns of cytotype distribution and genome size variation in the genus Sesleria Scop. (Poaceae). Bot J Linn Soc 179:126–143. https://doi.org/10.1111/boj.12306
Ledent A, Désamoré A, Laenen B, Mardulyn P, McDaniel SF, Zanatta F, Patiño J, Vanderpoorten A (2019) No borders during the post-glacial assembly of European bryophytes. Ecol Lett 22:973–986. https://doi.org/10.1111/ele.13254
López-González N, Bobo-Pinilla J, Padilla-García N, Loureiro J, Castro S, Rojas-Andrés BM, Martínez-Ortega MM (2021) Genetic similarities versus morphological resemblance: unraveling a polyploid complex in a Mediterranean biodiversity hotspot. Molec Phylogen Evol 155:107006. https://doi.org/10.1016/j.ympev.2020.107006
López-Vinyallonga S, López-Pujol J, Constantinidis T, Susanna A, Garcia-Jacas N (2015) Mountains and refuges: Genetic structure and evolutionary history in closely related, endemic Centaurea in continental Greece. Molec Phylogen Evol 92:243–254. https://doi.org/10.1016/j.ympev.2015.06.018
Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629. https://doi.org/10.1111/j.1558-5646.1991.tb04333.x
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, New Jersey
Magauer M, Schönswetter P, Jang T-S, Frajman B (2014) Disentangling relationships within the disjunctly distributed Alyssum ovirense/A. wulfenianum group (Brassicaceae), including description of a novel species from the north-eastern Alps. Bot J Linn Soc 176:486–505. https://doi.org/10.1111/boj.12214
Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, de Beaulieu J-L (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–222. https://doi.org/10.1111/j.1469-8137.2006.01740.x
Maguilla E, Escudero M, Jiménez-Lobato V, Díaz-Lifante Z, Andrés-Camacho C, Arroyo J (2021) Polyploidy expands the range of Centaurium (Gentianaceae). Frontiers Pl Sci 12:650551. https://doi.org/10.3389/fpls.2021.650551
Magyari EK, Chapman JC, Gaydarska B, Marinova E, Deli T, Huntley JP, Allen JRM, Huntley BT (2008) The ‘oriental’ component of the Balkan flora: evidence of presence on the Thracian Plain during the Weichselian late-glacial. J Biogeogr 35:865–883. https://doi.org/10.1111/j.1365-2699.2007.01849.x
Mai DH (1995) Tertiäre Vegetationsgeschichte Europas. G. Fischer, Jena, Stuttgart, New York
Manafzadeh S, Salvo G, Conti E (2014) A tale of migrations from east to west: the Irano-Turanian floristic region as a source of Mediterranean xerophytes. J Biogeogr 41:366–379. https://doi.org/10.1111/jbi.12185
Mansion G, Rosenbaum G, Schoenenberger N, Bacchetta G, Rosselló JA, Conti E (2008) Phylogenetic analysis informed by geological history supports multiple, sequential invasions of the Mediterranean basin by the angiosperm family Araceae. Syst Biol 57:269–285. https://doi.org/10.1080/10635150802044029
Marhold K (2011a onwards) Crassulaceae. In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Marhold K (2011b onwards) Scrophularia. In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York
Mayr E (1947) Ecological factors in speciation. Evolution 1:263–288. https://doi.org/10.1111/j.1558-5646.1947.tb02723.x
Melichárková A, Šlenker M, Zozomová-Lihová J, Skokanová K, Šingliarová B, Kačmárová T, Caboňová M, Kempa M, Šrámková G, Mandáková T, Lysák MA, Svitok M, Mártonfiová L, Marhold K (2020) So closely related and yet so different: strong contrasts between the evolutionary histories of species of the Cardamine pratensis polyploid complex in Central Europe. Frontiers Pl Sci 11:588856. https://doi.org/10.3389/fpls.2020.588856
Melichárková A, Španiel S, Brišková D, Marhold K, Zozomová-Lihová J (2017) Unravelling allopolyploid origins in the Alyssum montanum–A. repens (Brassicaceae) species complex: low-copy nuclear gene data complement cpDNA sequences and AFLPs. Bot J Linn Soc 184:485–502. https://doi.org/10.1093/botlinnean/box039
Melichárková A, Španiel S, Marhold K, Hurdu B-I, Drescher A, Zozomová-Lihová J (2019) Diversification and independent polyploid origins in the disjunct species Alyssum repens from the SE Alps and the Carpathians. Amer J Bot 106:1499–1518. https://doi.org/10.1002/ajb2.1370
Mereďa P, Hodálová I, Kučera J, Zozomová-Lihová J, Letz DR, Slovák M (2011) Genetic and morphological variation in Viola suavis s.l. (Violaceae) in the western Balkan Peninsula: two endemic subspecies revealed. Syst Biodivers 9:211–231. https://doi.org/10.1080/14772000.2011.603903
Meulenkamp JE, Sissingh W (2003) Tertiary palaeogeography and tectonostratigraphic evolution of the northern and southern peri-Tethys platforms and the intermediate domains of the African-Eurasian convergent plate boundary zone. Palaeogeogr Palaeoclimatol Palaeoecol 196:209–228. https://doi.org/10.1016/S0031-0182(03)00319-5
Milivojević M, Menković L, Ćalić J (2008) Pleistocene glacial relief of the central part of Mt. Prokletije (Albanian Alps). Quatern Int 190:112–122. https://doi.org/10.1016/j.quaint.2008.04.006
Moore AJ, Kadereit JW (2013) The evolution of substrate differentiation in Minuartia series Laricifoliae (Caryophyllaceae) in the European Alps: in situ origin or repeated colonisation? Amer J Bot 100:2412–2425. https://doi.org/10.3732/ajb.1300225
Moore AJ, Messick JA, Kadereit JW (2021) Range and niche expansion through multiple interspecific hybridization: a genotyping by sequencing analysis of Cherleria (Caryophyllaceae) BMC Ecol Evol 21:40. https://doi.org/10.1186/s12862-020-01721-5
Musacchio A, Pellegrino G, Cafasso D, Widmer A, Cozzolino S (2006) A unique A. palustris lineage across the Otranto strait: a botanical evidence for a past land-bridge? Pl Syst Evol 262:103–111. https://doi.org/10.1007/s00606-006-0469-y
Naciri Y, Gaudeul M (2007) Phylogeography of the endangered Eryngium alpinum L. (Apiaceae), in the European Alps. Molec Ecol 16:2721–2733. https://doi.org/10.1111/j.1365-294X.2007.03269.x
Natcheva R, Cronberg N (2003) Genetic diversity in populations of Sphagnum capillifolium from the mountains of Bulgaria, and their possible refugial role. J Bryol 25:91–99. https://doi.org/10.1179/037366803235001742
Nieto Feliner G (2014) Patterns and processes in plant phylogeography in the Mediterranean Basin: A review. Perspect Pl Ecol Evol Syst 16:265–278. https://doi.org/10.1016/j.ppees.2014.07.002
Nikolić T (ed) (2021) Flora Croatica Database. Sveučilište u Zagrebu, Prirodoslovno-matematički fakultet, Botanički zavod s botaničkim vrtom, Zagreb. Available at: http://hirc.botanic.hr/fcd/. Accessed 27 Sep 2021
Ninčević T, Jug‑Dujaković M, Grdiša M, Liber Z, Varga F, Pljevljakušić D, Šatović Z (2021) Population structure and adaptive variation of Helichrysum italicum (Roth) G. Don along eastern Adriatic temperature and precipitation gradient. Sci Rep 11:24333. https://doi.org/10.1038/s41598-021-03548-6
Oberprieler C (2005) Temporal and spatial diversification of circum-Mediterranean Compositae-Anthemidae. Taxon 54:951–966. https://doi.org/10.2307/25065480
Olšavská K, Slovák M, Marhold K, Štubňová E, Kučera J (2016) On the origins of Balkan endemics: the complex evolutionary history of the Cyanus napulifer group (Asteraceae). Ann Bot (Oxford) 118:1071–1088. https://doi.org/10.1093/aob/mcw142
Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462. https://doi.org/10.1016/j.cell.2007.10.022
Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annual Rev Genet 34:401–437. https://doi.org/10.1146/annurev.genet.34.1.401
Özüdoğru B, Mummenhoff K (2020) Phylogenetic and biogeographical history confirm the Anatolian origin of Bornmuellera (Brassicaceae) and clade divergence between Anatolia and the Balkans in the Plio-Pleistocene transition. Turkish J Bot 44:593–603. https://doi.org/10.3906/bot-2007-42
Panitsa M, Kagiampaki A, Kougioumoutzis K (2018) Plant diversity and biogeography of the Aegean Archipelago: a new synthesis. In: Moysis M, Pafilis P, Parmakelis A, Poulakakis N, Sfenthourakis S, Triantis K (eds) Biogeography and biodiversity of the Aegean. Broken Hill Publishers, Nicosia, In honour of Prof. Moysis Mylonas, pp 269–278
Park JM, Kovacic S, Liber Z, Eddie WM, Schneeweiss GM (2006) Phylogeny and biogeography of isophyllous species of Campanula (Campanulaceae) in the Mediterranean area. Syst Bot 31:862–880. https://doi.org/10.1600/036364406779695924
Paule J, Dunkel FG, Schmidt M, Gregor T (2018) Climatic differentiation in polyploid apomictic Ranunculus auricomus complex in Europe. BMC Ecol 18:16. https://doi.org/10.1186/s12898-018-0172-1
Perný M, Tribsch A, Anchev ME (2004) Infraspecific differentiation in the Balkan diploid Cardamine acris (Brassicaceae): molecular and morphological evidence. Folia Geobot 39:405–429. https://doi.org/10.1007/BF02803211
Perrino EV (2011) New data on Aegilops uniaristata Vis. in Italy. Nat Croat 20:117–123
Peruzzi L, Caparelli KF (2007) Gagea peduncularis (J. & C. Presl) Pascher (Liliaceae) new for the Italian flora. Webbia 62:261–268. https://doi.org/10.1080/00837792.2007.10670827
Petrova G, Moyankova D, Nishii K, Forrest L, Tsiripidis I, Drouzas AD, Djilianov D, Möller M (2015) The European paleoendemic Haberlea rhodopensis (Gesneriaceae) has an Oligocene origin and a Pleistocene diversification and occurs in a long-persisting refugial area in southeastern Europe. Int J Pl Sci 176:499–514. https://doi.org/10.1086/681990
Piotti A, Leonarduzzi C, Postolache D, Bagnoli F, Spanu I, Brousseau L, Urbinati C, Leonardi S, Vendramin GG (2017) Unexpected scenarios from Mediterranean refugial areas: disentangling complex demographic dynamics along the Apennine distribution of silver fir. J Biogeogr 44:1547–1558. https://doi.org/10.1111/jbi.13011
Popov SC, Shcherba IG, Ilyina LB, Nevesskaya LA, Paramonova NP, Khondkarian SO, Magyar I (2006) Late Miocene to Pliocene palaeogeography of the Paratethys and its relation to the Mediterranean. Palaeogeogr Palaeoclimatol Palaeoecol 238:91–106. https://doi.org/10.1016/j.palaeo.2006.03.020
Postolache D, Popescu F, Paule L, Ballian D, Zhelev P, Fărcaş S, Paule J, Badea O (2017) Unique postglacial evolution of the hornbeam (Carpinus betulus L.) in the Carpathians and the Balkan Peninsula revealed by chloroplast DNA. Sci Total Environm 599:1493–1502. https://doi.org/10.1016/j.scitotenv.2017.05.062
Ramsey J (2011) Polyploidy and ecological adaptation in wild yarrow. Proc Natl Acad Sci USA 108:7096–7101. https://doi.org/10.1073/pnas.1016631108
Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Rev Ecol Syst 29:467–501. https://doi.org/10.1146/annurev.ecolsys.29.1.467
Rapp D (2012) Ice Ages and Interglacials. Measurements, Interpretation, and Models. 2nd edn. Springer, Berlin, Heidelberg
Reed JM, Kryštufek B, Eastwood WJ (2004) The physical geography of the Balkans and nomenclature of place names. In: Griffiths HI, Krystufek B, Reed JM (eds) Balkan Biodiversity. Kluwer Academic Publishers, Dordrecht, pp 9–22
Reich D, Flatscher R, Pellegrino G, Hülber K, Wessely J, Gattringer A, Greimler J (2021) Biogeography of amphi-adriatic Gentianella crispata (Gentianaceae): a northern refugium and recent trans-adriatic migration. Pl Biosyst 156:754–768. https://doi.org/10.1080/11263504.2021.1918783
Rešetnik I, Baričević D, Batîr Rusu D, Carović-Stanko K, Chatzopoulou P, Dajić-Stevanović Z, Gonceariuc M, Grdiša M, Greguraš D, Ibraliu A, Jug-Dujaković M, Krasniqi E, Liber Z, Murtić S, Pećanac D, Radosavljević I, Stefkov G, Stešević D, Šoštarić I, Šatović Z (2016a) Genetic Diversity and Demographic History of Wild and Cultivated/Naturalised Plant Populations: Evidence from Dalmatian Sage (Salvia officinalis L., Lamiaceae). PLoS ONE 11:e0159545. https://doi.org/10.1371/journal.pone.0159545
Rešetnik I, Frajman B, Bogdanović S, Ehrendorfer F, Schönswetter P (2014) Disentangling relationships among the diploid members of the intricate genus Knautia (Caprifoliaceae, Dipsacoideae). Molec Phylogen Evol 74:97–110. https://doi.org/10.1016/j.ympev.2014.01.028
Rešetnik I, Frajman B, Schönswetter P (2016b) Heteroploid Knautia drymeia includes K. gussonei and cannot be separated into diagnosable subspecies. Amer J Bot 103:1300–1313. https://doi.org/10.3732/ajb.1500506
Rešetnik I, Temunović M, Liber Z, Satovic Z, Bogdanovic S (2020) Phylogeography of Campanula fenestrellata s.l. (Campanulaceae) in the northern Adriatic. Pl Syst Evol 306:42. https://doi.org/10.1007/s00606-020-01668-6
Rešetnik I, Záveská E, Grgurev M, Bogdanović S, Bartolić P, Frajman B (2022) Stability in the south, turbulence toward the north: evolutionary history of Aurinia saxatilis (Brassicaceae) revealed by phylogenomic and climatic modelling data. Frontiers Pl Sci 13:822331. https://doi.org/10.3389/fpls.2022.822331
Rögl F (1999) Mediterranean and Paratethys. Facts and hypotheses of an Oligocene to Miocene paleogeography (short overview). Geol Carpath 50:339–349
Rojas-Andrés BM, Albach DC, Martínez-Ortega MM (2015) Exploring the intricate evolutionary history of the diploid–polyploid complex Veronica subsection Pentasepalae (Plantaginaceae). Bot J Linn Soc 179:670–692. https://doi.org/10.1111/boj.12345
Rojas-Andrés BM, Padilla-García N, Pedro MD, López-González N, Delgado L, Albach DC, Castro M, Castro S, Loureiro J, Martínez-Ortega MM (2020) Environmental differences are correlated with the distribution pattern of cytotypes in Veronica subsection Pentasepalae at a broad scale. Ann Bot (Oxford) 125:471–484. https://doi.org/10.1093/aob/mcz182
Ronikier M, Zalewska-Gałosz J (2014) Independent evolutionary history between the Balkan ranges and more northerly mountains in Campanula alpina s.l. (Campanulaceae): Genetic divergence and morphological segregation of taxa. Taxon 63:116–131. https://doi.org/10.12705/631.4
Roquet C, Sanmartín I, Garcia-Jacas N, Sáez L, Susanna A, Wikström N, Aldasoro JJ (2009) Reconstructing the history of Campanulaceae with a Bayesian approach to molecular dating and dispersal–vicariance analyses. Molec Phylogen Evol 52:575–587. https://doi.org/10.1016/j.ympev.2009.05.014
Rosati L, Coppi A, Farris E, Fascetti S, Becca G, Peregrym M, Tan K, Selvi F (2019) The genus Gymnospermium (Berberidaceae) in Italy: Identity and relationships of the populations at the western limit of the genus range. Pl Biosyst 153:796–808. https://doi.org/10.1080/11263504.2018.1549613
Rothfels CJ, Pryer KM, Li FW (2017) Next-generation polyploid phylogenetics: rapid resolution of hybrid polyploid complexes using PacBio single-molecule sequencing. New Phytol 213:413–429. https://doi.org/10.1111/nph.14111
Rouchy JM, Caruso A (2006) The Messinian salinity crisis in the Mediterranean basin: a reassessment of the data and an integrated scenario. Sediment Geol 188–189:35–67. https://doi.org/10.1016/j.sedgeo.2006.02.005
Runemark H (1980) Studies in the Aegean Flora XXIII. The Dianthus fruticosus complex (Caryophyllaceae). Bot Not 133:475–490
Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford
Schmickl R, Liston A, Zeisek V, Oberlander K, Weitemier K, Straub SCK, Cronn RC, Dreyer LL, Suda J (2016) Phylogenetic marker development for target enrichment from transcriptome and genome skim data: the pipeline and its application in southern African Oxalis (Oxalidaceae). Molec Ecol Resources 16:1124–1135. https://doi.org/10.1111/1755-0998.12487
Schönswetter P, Schneeweiss GM (2009) Androsace komovensis sp. nov., a long mistaken local endemic from the southern Balkan Peninsula with biogeographic links to the Eastern Alps. Taxon 58:544–549. https://doi.org/10.1002/tax.582018
Schönswetter P, Tribsch A (2005) Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae). Taxon 54:725–732. https://doi.org/10.2307/25065429
Sikora M, Mihanović H, Vilibić I (2014) Paleo-coastline of the Central Eastern Adriatic Sea, and Paleo-Channels of the Cetina and Neretva rivers during the last glacial maximum. Acta Adriat 55:3–18
Siljak-Yakovlev S, Stevanović V, Tomasević M, Brown SC, Stevanović B (2008) Genome size variation and polyploidy in the resurrection plant genus Ramonda: cytogeography of living fossils. Environm Exp Bot 62:101–112. https://doi.org/10.1016/j.envexpbot.2007.07.017
Simaiakis SM, Rijsdijk KF, Koene EFM, Norder SJ, Van Boxel JH, Stocchi P, Hammoud C, Kougioumoutzis K, Georgopoulou E, van Loon E, Tjørve KMC, Tjørve E (2017) Geographic changes in the Aegean Sea since the Last Glacial Maximum: Postulating biogeographic effects of sea-level rise on islands. Palaeogeogr Palaeoclimatol Palaeoecol 471:108–119. https://doi.org/10.1016/j.palaeo.2017.02.002
Simpson GG (1953) The major features of evolution. Columbia University Press, New York
Šingliarová B, Hodalová I, Mráz P (2011) Biosystematic study of the diploid-polyploid Pilosella alpicola group with variation in breeding system: patterns and processes. Taxon 60:450–470. https://doi.org/10.1002/tax.602014
Skokanová K, Hodálová I, Mereďa P, Slovák M, Kučera J (2019a) The Cyanus tuberosus group (Asteraceae) in the Balkans: biological entities require correct names. Pl Syst Evol 305:569–596. https://doi.org/10.1007/s00606-019-01576-4
Skokanová K, Šingliarová B, Kochjarová J, Paule J (2019b) Nuclear ITS and AFLPs provide surprising implications for the taxonomy of Tephroseris longifolia agg. and the endemic status of T. longifolia subsp. moravica. Pl Syst Evol 305:865–884. https://doi.org/10.1007/s00606-019-01624-z
Skubic M, Schönswetter P, Frajman B (2018) Diversification of Cerastium sylvaticum and C. subtriflorum on the margin of the south-eastern Alps. Pl Syst Evol 304:1101–1115. https://doi.org/10.1007/s00606-018-1535-y
Šlenker M, Kantor A, Marhold K, Schmickl R, Mandáková T, Lysak MA, Perný M, Caboňová M, Slovák M, Zozomová-Lihová J (2021) Allele sorting as a novel approach to resolving the origin of allotetraploids using Hyb-Seq data: A case study of the Balkan mountain endemic Cardamine barbaraeoides. Frontiers Pl Sci 12:659275. https://doi.org/10.3389/fpls.2021.659275
Slovák M, Kučera J, Turis P, Zozomová-Lihová J (2012) Multiple glacial refugia and postglacial colonization routes inferred for a woodland geophyte, Cyclamen purpurascens: Patterns concordant with the Pleistocene history of broadleaved and coniferous tree species. Biol J Linn Soc 105:741–760. https://doi.org/10.1111/j.1095-8312.2011.01826.x
Sobierajska K, Boratyńska K, Jasińska A, Dering M, Ok T, Douaihy B, Bou Dagher-Kharrat M, Romo Á, Boratyński A (2016) Effect of the Aegean Sea barrier between Europe and Asia on differentiation in Juniperus drupacea (Cupressaceae). Bot J Linn Soc 180:365–385. https://doi.org/10.1016/j.ympev.2015.06.018
Sochor M, Trávníček B, Király G (2019) Ploidy level variation in the genus Rubus in the Pannonian Basin and the northern Balkans, and evolutionary implications. Pl Syst Evol 305:611–626. https://doi.org/10.1007/s00606-019-01593-3
Soltis PS, Liu X, Marchant DB, Visger CJ, Soltis DE (2014) Polyploidy and novelty: Gottlieb’s legacy. Philos Trans Roy Soc London B Biol Sci 369:20130351. https://doi.org/10.1098/rstb.2013.0351
Soltis PS, Marchant DB, Van de Peer Y, Soltis DE (2015) Polyploidy and genome evolution in plants. Curr Opin Genet Developm 35:119–125. https://doi.org/10.1016/j.gde.2015.11.003
Soltis DE, Soltis PS, Schemske DW, Hancock JF, Thompson JN, Husband BC, Judd WS (2007) Autopolyploidy in angiosperms: Have we grossly underestimated the number of species? Taxon 56:13–30. https://doi.org/10.2307/25065732
Španiel S, Juillerat P, Kaplan K, Bovio M, Bäumler B, Perret M, Mártonfiová L, Zozomová-Lihová J. (2022) Out of the Balkans and Anatolia to the Western Alps? Surprising phylogenetic implications for two endemic Alyssum (Brassicaceae) species: A. cognense sp. nov. and A. rossetii. Bot J Linn Soc (in press)
Španiel S, Marhold K, Zozomová-Lihová J (2017a) The polyploid Alyssum montanum-A. repens complex in the Balkans: a hotspot of species and genetic diversity. Pl Syst Evol 303:1443–1465. https://doi.org/10.1007/s00606-017-1470-3
Španiel S, Zozomová-Lihová J, Marhold K (2017b) Revised taxonomic treatment of the Alyssum montanum-A. repens complex in the Balkans: a multivariate morphometric analysis. Pl Syst Evol 303:1413–1442. https://doi.org/10.1007/s00606-017-1468-x
Stachurska-Swakoń A, Cieślak E, Ronikier M (2012) Phylogeography of subalpine tall-herb species in Central Europe: the case of Cicerbita alpina (L.) Wallr. Preslia 84:121–140
Stachurska-Swakoń A, Cieślak E, Ronikier M (2013) Phylogeography of a subalpine tall-herb Ranunculus platanifolius (Ranunculaceae) reveals two main genetic lineages in the European mountains. Bot J Linn Soc 171:413–428. https://doi.org/10.1111/j.1095-8339.2012.01323.x
Stachurska-Swakoń A, Cieślak E, Ronikier M, Nowak J, Kaczmarczyk A (2020) Genetic structure of Doronicum austriacum (Asteraceae) in the Carpathians and adjacent areas: toward a comparative phylogeographical analysis of tall-herb species. Pl Syst Evol 306:14. https://doi.org/10.1007/s00606-020-01652-0
Stefanović S, Lakušić D, Kuzmina M, Međedović S, Tan K, Stevanović V (2008) Molecular phylogeny of Edraianthus (Grassy Bells; Campanulaceae) based on non-coding plastid DNA sequences. Taxon 57:452–475. https://www.jstor.org/stable/25066015
Steininger FF, Rögl F (1984) Paleogeography and palinspastic reconstruction of the Neogene of the Mediterranean and Paratethys. In: Dixon JE, Robertson AHF (eds) The Geological Evolution of the Eastern Mediterranean. The Geological Society, London, pp 659–669
Stešević D, Caković D (2013) Catalogue of vascular flora of Montenego. Crnogorska akademija nauka i umjetnosti, Podgorica
Stevanoski I, Kuzmanović N, Dolenc Koce J, Schönswetter P, Frajman B (2020) Disentangling relationships between amphi-Adriatic Euphorbia spinosa and Balkan endemic E. glabriflora (Euphorbiaceae). Bot J Linn Soc 194:358–374. https://doi.org/10.1093/botlinnean/boaa032
Stevanović V, Tan K, Iatrou G (2003) Distribution of the endemic Balkan flora on serpentine I.-Obligate serpentine endemics. Pl Syst Evol 242:149–170. https://doi.org/10.1007/s00606-003-0044-8
Stevanović V, Tan K, Petrova A (2007) Mapping the endemic flora of the Balkans—a progress report. Bocconea 21:131–137
Strid A (1993) Phytogeographical aspects of the Greek mountain flora. Fragm Florist Geobot, Suppl 2:411–433
Strid A (1996) Phytogeographia Aegaea and the Flora Hellenica database. Ann Naturhist Mus Wien, B 98(Suppl):279–289
Strid A (2016) Atlas of the Aegean Flora. Botanic Garden and Botanical Museum Berlin, Berlin
Strid A (2020) The botanical exploration of Greece. Pl Syst Evol 306:27. https://doi.org/10.1007/s00606-020-01637-z
Strid A, Andonoski A, Andonovski V (2003) The High Mountain Vegetation of the Balkan Peninsula. In: Nagy L, Grabherr G, Körner Ch, Thompson DBA (eds) Alpine biodiversity in Europe. Ecological Studies, vol. 167. Springer-Verlag, Berlin, Heidelberg, pp 113–121
Suarez-Gonzalez A, Lexer C, Cronk QCB (2018) Adaptive introgression: a plant perspective. Biol Lett 14:20170688. https://doi.org/10.1098/rsbl.2017.0688
Suc J-P (1984) Origin and evolution of the Mediterranean vegetation and climate in Europe. Nature 307:429–432. https://www.nature.com/articles/307429a0
Surina B, Pfanzelt S, Einzmann HJR, Albach, DC (2014a) Bridging the Alps and the Middle East: evolution, phylogeny and systematics of the genus Wulfenia (Plantaginaceae). Taxon 63:843–858. https://doi.org/10.12705/634.18
Surina B, Schneeweiss GM, Glasnović P, Schönswetter P (2014b) Testing the efficiency of nested barriers to dispersal in the Mediterranean high mountain plant Edraianthus graminifolius (Campanulaceae). Molec Ecol 23:2861–2875. https://doi.org/10.1111/mec.12779
Surina B, Schönswetter P, Schneeweiss GM (2011) Quarternary range dynamics of ecologically divergent species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan refugium. J Biogeogr 38:1381–1393. https://doi.org/10.1111/j.1365-2699.2011.02493.x
Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson 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
Tate JA, Soltis DE, Soltis PS (2005) Polyploidy in plants. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, California, USA, pp 371–426
Temunović M, Franjić J, Satovic Z, Grgurev M, Frascaria-Lacoste N, Fernández-Manjarrés JF (2012) Environmental heterogeneity explains the genetic structure of Continental and Mediterranean populations of Fraxinus angustifolia Vahl. PLoS ONE 7:e42764. https://doi.org/10.1371/journal.pone.0042764
Terlević A, Bogdanović S, Frajman B, Rešetnik I (2022) Genome Size Variation in Dianthus sylvestris Wulfen sensu lato (Caryophyllaceae). Plants 11:1481. https://doi.org/10.3390/plants11111481
Thomas CD, Franco AMA, Hill JK (2006) Range retractions and extinction in the face of climate warming. Trends Ecol Evol 21:415–416. https://doi.org/10.1016/j.tree.2006.05.012
Thompson JD (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford
Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hübner S, Heredia SM, Hahn MA, Caseys C, Bock DG, Rieseberg LH (2016) Hybridization and Extinction. Evol Applic 9:892–908. https://doi.org/10.1111/eva.12367
Tomović G, Niketić M, Lakušić D, Ranđelović V, Stevanović V (2014) Balkan endemic plants in Central Serbia and Kosovo regions: distribution patterns, ecological characteristics, and centres of diversity. Bot J Linn Soc 176:173–202. https://doi.org/10.1111/boj.12197
Trewick SA, Morgan-Richards M, Russel l SJ, Henderson S, Rumsey FJ, Pinter I, Barret A, Gibby M, Vogel JC, (2002) Polyploidy, phylogeography and Pleistocene refugia of the rockfern Asplenium ceterach: evidence from chloroplast DNA. Molec Ecol 11:2003–2012. https://doi.org/10.1046/j.1365-294x.2002.01583.x
Trotter A (1912) Gli elementi Balcanico-Orientali della Flora Italiana e l’ipotesi dell’ ‘Adriatide.’ Atti Reale Ist Incoragg Napoli, Ser VI 9:1–119
Turrill WB (1929) The plant life of the Balkan peninsula: a phytogeographical study. Clarendon, Oxford
Tzedakis PC, Lawson IT, Frogley MR, Hewitt GM, Preece RC (2002) Buffered tree population changes in a Quaternary refugium: evolutionary implications. Science 297:2044–2047. https://doi.org/10.1126/science.1073083
Valdés B (2009 onwards) Erica. In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Valdés B, Scholz H (2009) Poaceae (pro parte majore). In: Euro+Med Plantbase – the information resource for Euro-Mediterranean plant diversity. Available at: http://ww2.bgbm.org/euroPlusMed/query.asp. Accessed 26 May 2020
Vargas P, Fernandez-Mazuecos M, Heleno R (2017) Phylogenetic evidence for a Miocene origin of Mediterranean lineages: species diversity, reproductive traits and geographical isolation. Pl Biol (Stuttgart) 20:157–165. https://doi.org/10.1111/plb.12626
Vižintin L, Kosovel V, Feoli Chiapella L, Bohanec B (2012) Genetic characterization of Genista sericea Wulfen (Cytiseae-Fabaceae) as revealed by nuclear DNA content and ITS nrDNA region analysis. Acta Bot Croat 71:195–205. https://doi.org/10.2478/v10184-012-0003-y
Wagensommer RP, Bartolucci F, Forentino M, Licht W, Peccenini S, Perrino EV, Venanzoni R (2017) First record for the flora of Italy and lectotypification of the name Linum elegans (Linaceae). Phytotaxa 296:161–170. https://doi.org/10.11646/phytotaxa.296.2.5
Wagensommer RP, Fröhlich T, Fröhlich M (2014) First record of the southeast European species Cerinthe retorta Sibth. & Sm. (Boraginaceae) in Italy and considerations on its distribution and conservation status. Acta Bot Gallica 161:111–115. https://doi.org/10.1080/12538078.2014.892438
Whitney KD, Randell RA, Rieseberg LH (2010) Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol 187:230–239. https://doi.org/10.1111/j.1469-8137.2010.03234.x
Willis KJ (1994) The vegetational history of the Balkans. Quatern Sci Rev 13:769–788. https://doi.org/10.1016/0277-3791(94)90104-X
Willner W, Di Pietro R, Bergmeier E (2009) Phytogeographical evidence for post-glacial dispersal limitation of European beech forest species. Ecography 32:1011–1018. https://doi.org/10.1111/j.1600-0587.2009.05957.x
Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106:13875–13879. https://doi.org/10.1073/pnas.0811575106
Yakimowski SB, Rieseberg LH (2014) The role of homoploid hybridization in evolution: a century of studies synthesizing genetics and ecology. Amer J Bot 101:1247–1258. https://doi.org/10.3732/ajb.1400201
Záveská E, Maylandt C, Paun O, Bertel C, Frajman B, The STEPPE Consortium, Schönswetter P (2019) Multiple auto- and allopolyploidisations marked the Pleistocene history of the widespread Eurasian steppe plant Astragalus onobrychis (Fabaceae). Molec Phylogen Evol 139:106572. https://doi.org/10.1016/j.ympev.2019.106572
Záveská E, Kirschner P, Frajman B, Wessely J, Willner W, Gattringer A, Hülber K, Lazić D, Dobeš C, Schönswetter P (2021) Evidence for glacial refugia of the forest understorey Species Helleborus niger (Ranunculaceae) in the Southern as well as in the Northern Limestone Alps. Frontiers Pl Sci 12:683043. https://doi.org/10.3389/fpls.2021.683043
Zozomová-Lihová J, Melichárková A, Svitok M, Španiel S (2020) Pleistocene range disruption and postglacial expansion with secondary contacts explain genetic and cytotype structure in the western Balkan endemic Alyssum austrodalmaticum (Brassicaceae). Pl Syst Evol 306:47. https://doi.org/10.1007/s00606-020-01677-5
Zozomová-Lihová J, Marhold K, Španiel S (2014) Taxonomy and evolutionary history of Alyssum montanum (Brassicaceae) and related taxa in southwestern Europe and Morocco: diversification driven by polyploidy, geographic and ecological isolation. Taxon 63:562–591. https://doi.org/10.12705/633.18
Acknowledgements
We thank the two anonymous reviewers for their valuable general and specific comments for improving the quality of the paper. The work of SŠ was financially supported by the Slovak Research and Development Agency (APVV; Grant No. APVV-17-0616), and Grant Agency VEGA, Bratislava, Slovakia (Grant No. 2/0022/21), while the work of IR was supported by Croatian Science Foundation (Grant No. UIP-2017-05-2882).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Marcus Koch.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contribution to “Plants of the Balkan Peninsula in Space and Time”.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Španiel, S., Rešetnik, I. Plant phylogeography of the Balkan Peninsula: spatiotemporal patterns and processes. Plant Syst Evol 308, 38 (2022). https://doi.org/10.1007/s00606-022-01831-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-022-01831-1