Abstract
In the context of Europe, the southern peninsulas including the Balkans are considered hotspots of diversity. They preserved substantial parts of tree species and genera occurring in Europe during the Tertiary, as the effects of the Quaternary glaciations on species richness were not as severe here as in more northerly regions. The Balkans also harboured glacial refugia of most European trees, and this was probably the reason for a premature suggestion that this region was the main source for the Holocene recolonization of Central and Eastern Europe. However, studies based on a combination of paleobotanical and genetic evidence showed that this was an exception rather than a rule. In most tree species, the Balkan refugia have not effectively contributed to current gene pools. In spite of this, empirical studies have documented that genetic diversity in the Balkan region is generally higher than elsewhere in Europe, which can be attributed to a high number of refugia in this area harbouring differentiated genetic lineages, and high environmental heterogeneity. This makes the Balkans an important source of genetic material for forestry, especially in the light of the ongoing climate change.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen JRM, Hickler T, Singarayer JS, Sykes MT, Valdes PJ, Huntley B (2010) Last glacial vegetation of northern Eurasia. Quatern Sci Rev 29:2604–2618. https://doi.org/10.1016/j.quascirev.2010.05.031
Binney H, Edwards M, Macias-Fauria M, Lozhkin A, Anderson P, Kaplan JO, Andreev A, Bezrukova E, Blyakharchuk T, Jankovska V, Khazina I, Krivonogov S, Kremenetski K, Nield J, Novenko E, Ryabogina N, Solovieva N, Willis K, Zernitskaya V (2017) Vegetation of Eurasia from the last glacial maximum to present: key biogeographic patterns. Quatern Sci Rev 157:80–97. https://doi.org/10.1016/j.quascirev.2016.11.022
Birks HJB, Tinner W (2016) Past forests of Europe. In: San Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A (eds) European Atlas of Forest Tree Species, vol. 197, p e010c45+. Publication Office of the EU, Luxembourg
Birks HJB, Willis KJ (2008) Alpines, trees, and refugia in Europe. Pl Ecol Divers 1:147–160. https://doi.org/10.1080/17550870802349146
Bošeľa M, Popa I, Gömöry D, Longauer R, Tobin B, Kyncl J, Kyncl T, Nechita C, Petráš R, Sidor CG, Šebeň V, Büntgen U (2016) Effects of post-glacial phylogeny and genetic diversity on the growth variability and climate sensitivity of European silver fir. J Ecol 104:716–724. https://doi.org/10.1111/1365-2745.12561
Brus R (2010) Growing evidence for the existence of glacial refugia of European beech (Fagus sylvatica L.) in the south-eastern Alps and north-western Dinaric Alps. Period Biol 112:239–246
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
Cheddadi R, de Beaulieu J-L, Jouzel J, Andrieu-Ponel V, Laurent J-M, Reille M, Raynaud D, Bar-Hen A (2005) Similarity of vegetation dynamics during interglacial periods. Proc Natl Acad Sci USA 102:13939–13943. https://doi.org/10.1073/pnas.0501752102
Comps B, Gömöry D, Letouzey J, Thiébaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397
Cornille A, Giraud T, Bellard C, Tellier A, le Cam B, Smulders MJM, Kleinschmit J, Roldan-Ruiz I, Gladieuc P (2013) Postglacial recolonization history of the European crabapple (Malus sylvestris Mill.): a wild contributor to the domesticated apple. Molec Ecol 22:2249–2263. https://doi.org/10.1111/mec.12231
Czeczott H (1933) Studium nad zmiennością liści buków: Fagus orientalis Lipsky, F. sylvatica L. i form pośrednich. Rocz Dendrol 5:45–121
Donohue I, Petchey OL, Montoya JM, Jackson AL, McNally L, Viana M, Healy K, Lurgi M, O’Connor NE, Emmerson MC (2013) On the dimensionality of ecological stability. Ecol Lett 16:421–429. https://doi.org/10.1111/ele.12086
Dounavi A, Netzer F, Celepirović N, Ivanković M, Burger J, Figueroa AG, Schon S, Simon J, Cremer E, Fussi B, Konnert M, Rennenberg H (2016) Genetic and physiological differences of European beech provenances (F. sylvatica L.) exposed to drought stress. Forest Ecol Managem 361:226–236. https://doi.org/10.1016/j.foreco.2015.11.014
Fineschi S, Anzidei M, Cafasso D, Cozzolino S, Garfì G, Pastorelli R, Salvini D, Taurchini D, Vendramin GG (2002) Molecular markers reveal a strong genetic differentiation between two European relic tree species: Zelkova abelicea (Lam.) Boissier and Z. sicula Di Pasquale, Garfì and Quézel (Ulmaceae). Conservation Genet 3:145–153. https://doi.org/10.1023/A:1015222230887
Follieri M, Magri D, Sadori L (1986) Late Pleistocene Zelkova extinction in central Italy. New Phytol 103:269–273. https://doi.org/10.1111/j.1469-8137.1986.tb00613.x
George JP, Konrad H, Collin E, Thevenet J, Ballian D, Idzojtic M, Kamm U, Zhelev P, Geburek T (2015) High molecular diversity in the true service tree (Sorbus domestica) despite rareness: data from Europe with special reference to the Austrian occurrence. Ann Bot (Oxford) 115:1105–1115. https://doi.org/10.1093/aob/mcv047
Gérard PR, Temunović M, Sannier J, Bertolino P, Dufour J, Frascaria-Lacoste N, Fernandez-Manjarres JF (2013) Chilled but not frosty: understanding the role of climate in the hybridization between the Mediterranean Fraxinus angustifolia Vahl and the temperate Fraxinus excelsior L. (Oleaceae) ash trees. J Biogeogr 40:835–846. https://doi.org/10.1111/jbi.12021
Giesecke T, Brewer S (2018) Notes on the postglacial spread of abundant European tree taxa. Veget Hist Archaeobot 27:337–349. https://doi.org/10.1007/s00334-017-0640-0
Gömöry D, Longauer R, Liepelt S, Ballian D, Brus R, Kraigher H, Parpan VI, Parpan TV, Paule L, Stupar VI, Ziegenhagen B (2004) Variation patterns of mitochondrial DNA of Abies alba Mill. in suture zones of postglacial migration in Europe. Acta Soc Bot Pol 73:203–206. https://doi.org/10.5586/asbp.2004.027
Gömöry D, Paule L, Vyšný J (2007) Patterns of allozyme variation in western-Eurasian beeches. Bot J Linn Soc 154:165–174. https://doi.org/10.1111/j.1095-8339.2007.00666.x
Grivet D, Petit RJ (2003) Chloroplast DNA phylogeography of the hornbeam in Europe: evidence for a bottleneck at the outset of postglacial colonization. Conservation Genet 4:47–56. https://doi.org/10.1023/A:1021804009832
Harter DEV, Nagy L, Backhaus S, Beierkuhnlein C, Fussi B, Huber G, Jentsch A, Konnert M, Thiel D, Kreyling J (2015) A comparison of genetic diversity and phenotypic plasticity among European beech (Fagus sylvatica L.) populations from Bulgaria and Germany under drought and temperature manipulation. Int J Pl Sci 176:232–244. https://doi.org/10.1086/679349
Hatziskakis S, Papageorgiou AC, Gailing O, Finkeldey R (2009) High chloroplast haplotype diversity in Greek populations of beech (Fagus sylvatica L.). Pl Biol 11:425–433. https://doi.org/10.1111/j.1438-8677.2008.00111.x
Havrdová A, Douda J, Krak K, Vít P, Hadincová V, Zákravský P, Mandák B (2015) Higher genetic diversity in recolonized areas than in refugia of Alnus glutinosa triggered by continent-wide lineage admixture. Molec Ecol 24:4759–4777. https://doi.org/10.1111/mec.13348
Heuertz M, Hausman JF, Hardy OJ, Vendramin GG, Frascaria-Lacoste N, Vekemans X (2004a) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution 58:976–988. https://doi.org/10.1111/j.0014-3820.2004.tb00432.x
Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, Frascaria-Lacoste N, Hardy OJ, Vekemans X, Vendramin GG (2004b) Chloroplast DNA variation and postglacial recolonisation of common ash (Fraxinus excelsior L.) in Europe. Molec Ecol 13:3437–3452. https://doi.org/10.1111/j.1365-294X.2004.02333.x
Heuertz M, Carnevale S, Fineschi S, Sebastiani F, Hausman JF, Paule L, Vendramin GG (2006) Chloroplast DNA phylogeography of European ashes, Fraxinus sp (Oleaceae): roles of hybridization and life history traits. Molec Ecol 15:2131–2140. https://doi.org/10.1111/j.1365-294X.2006.02897.x
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276. https://doi.org/10.1111/j.1095-8312.1996.tb01434.x
Hewitt GM (2011) Mediterranean peninsulas: the evolution of hotspots. In: Frank E, Zachos FE, Habel JC (eds) Biodiversity hotspots. Distribution and protection of conservation. Springer, Berlin, pp 123–147. https://doi.org/10.1007/978-3-642-20992-5_7
Holm SR, Svenning J-C (2014) 180,000 Years of climate change in Europe: avifaunal responses and vegetation implications. PLoS ONE 9:e94021. https://doi.org/10.1371/journal.pone.0094021
Huntley B (1993) Species-richness in north-temperate zone forests. J Biogeogr 20:163–180. https://doi.org/10.2307/2845669
Kannenberg N, Gross K (1999) Allozymic variation in some Norway spruce populations of the international IUFRO provenance-testing programme of 1964/1968. Silvae Genet 48:209–217
Kovar-Eder J (2003) Vegetation dynamics in Europe during the Neogene. Deinsea 10:373–392
Kučerová V, Honec M, Paule L, Zhelev P, Gömöry D (2010) Genetic differentiation of Sorbus torminalis in Eastern Europe as determined by microsatellite markers. Biologia 65:817–821. https://doi.org/10.2478/s11756-010-0082-y
Lang G (1994) Quartäre Vegetationsgeschichte Europas: Methoden und Ergebnisse. Gustav Fischer Verlag, Jena
Liepelt S, Bialozyt R, Ziegenhagen B (2002) Wind-dispersed pollen mediates postglacial gene flow among refugia. Proc Natl Acad Sci USA 99:14590–14594. https://doi.org/10.1073/pnas.212285399
Liepelt S, Chedaddi R, de Beaulieu J-L, Fady B, Gömöry D, Hussendörfer E, Konnert M, Litt T, Longauer R, Terhürne-Berson R, Ziegenhagen B (2009) Biogeographic history of Abies alba Mill.: a synthesis from paleobotanic and genetic data. Rev Palaeobot Palynol 153:139–149. https://doi.org/10.1111/j.1365-2699.2006.01665.x
Magri D (2010) Persistence of tree taxa in Europe and Quaternary climate changes. Quatern Int 219:145–151. https://doi.org/10.1016/j.quaint.2009.10.032
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
Magri D, Di Rita F, Arabarri Erkiaga J, Fletcher W, González Sampériz P (2017) Quaternary disappearance of tree taxa from Southern Europe: timing and trends. Quatern Sci Rev 163:23–55. https://doi.org/10.1016/j.quascirev.2017.02.014
Mai DH (1995) Tertiäre Vegetationsgeschichte Europas: Methoden und Ergebnisse. Gustav Fischer Verlag, Jena
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
Mandák B, Havrdová A, Krak K, Hadincová V, Vit P, Zákravský P, Douda J (2016) Recent similarity in distribution ranges does not mean a similar postglacial history: a phylogeographical study of the boreal tree species Alnus incana based on microsatellite and chloroplast DNA variation. New Phytol 210:1395–1407. https://doi.org/10.1111/nph.13848
Martinetto E (2001) The role of central Italy as a centre of refuge for thermophilous plants in the late Cenozoic. Acta Palaeobot 41:299–319
Mayol M, Riba M, González-Martínez SC, Bagnoli F, de Beaulieu JL, Berganzo E, Burgarella C, Dubreuil M, Krajmerová D, Paule L, Romšáková I, Vettori C, Vincenot L, Vendramin GG (2015) Adapting through glacial cycles: insights from a long-lived tree (Taxus baccata). New Phytol 208:973–986. https://doi.org/10.1111/nph.13496
Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345. https://doi.org/10.1111/j.1365-2699.2008.02051.x
Neophytou C, Aravanopoulos FA, Fink S, Dounavi A (2010) Detecting interspecific and geographic differentiation patterns in two interfertile oak species (Quercus petraea (Matt.) Liebl. and Q. robur L.) using small sets of microsatellite markers. Forest Ecol Managem 259:2026–2035. https://doi.org/10.1016/j.foreco.2010.02.013
Nieto Feliner G (2011) Southern European glacial refugia: a tale of tales. Taxon 65:365–372. https://doi.org/10.1002/tax.602007
Palmé AE, Vendramin GG (2002) Chloroplast DNA variation, postglacial recolonization and hybridization in hazel, Corylus avellana. Molec Ecol 11:1769–1779. https://doi.org/10.1046/j.1365-294X.2002.01581.x
Palmé AE, Su Q, Rautenberg A, Manni F, Lascoux M (2003) Postglacial recolonization and cpDNA variation of silver birch, Betula pendula. Molec Ecol 12:201–212. https://doi.org/10.1046/j.1365-294X.2003.01724.x
Papageorgiou AC, Tsiripidis I, Mouratidis T, Hatziskakis S, Gailing O, Eliades NGH, Vidalis A, Drouzas AD, Finkeldey R (2014) Complex fine-scale phylogeographical patterns in a putative refugial region for Fagus sylvatica (Fagaceae). Bot J Linn Soc 174:516–528. https://doi.org/10.1111/boj.12148
Papi RM, Spanos KA, Kyriakidis DA (2012) Genetic variation of Fraxinus angustifolia natural populations in Greece based on nuclear and chloroplast microsatellite markers. Eur J Forest Res 131:1151–1161. https://doi.org/10.1007/s10342-011-0586-1
Pennekamp F, Pontarp M, Tabi A, Altermatt F, Alther R, Choffat Y, Fronhofer EA, Ganesanandamoorthy P, Garnier A, Griffiths JI, Greene S, Horgan K, Massie TM, Machler E, Palamara GM, Seymour M, Petchey OL (2018) Biodiversity increases and decreases ecosystem stability. Nature 563:109. https://doi.org/10.1038/s41586-018-0627-8
Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, Van Dam B, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz IG, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Popescu F, Slade D, Tabbenerg H, de Vries SGM, Ziegenhagen B, de Beaulieu J-L, Kremer A (2002) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol Managem 156:49–74. https://doi.org/10.1016/s0378-1127(01)00634-x
Petit RJ, Aguinagalde I, De Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565. https://doi.org/10.1126/science.1083264
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
Poljak I, Idžojtić M, Šatović Z, Ježić M, Ćurković-Perica M, Simovski B, Acevski J, Liber Z (2017) Genetic diversity of the sweet chestnut (Castanea sativa Mill.) in Central Europe and the western part of the Balkan Peninsula and evidence of marron genotype introgression into wild populations. Tree Genet Genomes 13:18. https://doi.org/10.1007/s11295-017-1107-2
Popescu SM, Biltekin D, Winter H, Suc JP, Melinte-Dobrinescu MC, Klotz S, Rabineau M, Combourieu-Nebout N, Clauzon G, Deaconu F (2010) Pliocene and lower Pleistocene vegetation and climate changes at the European scale: long pollen records and climatostratigraphy. Quatern Int 219:152–167. https://doi.org/10.1016/j.quaint.2010.03.013
Postolache D, Popescu F, Paule L, Ballian D, Zhelev P, Farcas 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 599–560:1493–1502. https://doi.org/10.1016/j.scitotenv.2017.05.062
Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genomes 4:247–254. https://doi.org/10.1007/s11295-007-0105-1
San Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A (eds) (2016) European Atlas of Forest Tree Species. Publication Office of the European Union, Luxembourg. 10.2788/425
Svenning J-C (2003) Deterministic Plio-Pleistocene extinctions in the European cool-temperate tree flora. Ecol Lett 6:646–653. https://doi.org/10.1046/j.1461-0248.2003.00477.x
Svenning J-C, Skov F (2007) Ice age legacies in the geographical distribution of tree species richness in Europe. Global Ecol Biogeogr 16:234–245. https://doi.org/10.1111/j.1466-8238.2006.00280.x
Taberlet P, Cheddadi R (2002) Quaternary refugia and persistence of biodiversity. Science 297:2009–2010. https://doi.org/10.1126/science.297.5589.2009
Taberlet P, Fumagalli L, Wust-Saucy AG, 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
Tollefsrud MM, Latalowa M, van der Knaap WO, Brochmann C, Sperisen C (2015) Late Quaternary history of North Eurasian Norway spruce (Picea abies) and Siberian spruce (Picea obovata) inferred from macrofossils, pollen and cytoplasmic DNA variation. J Biogeogr 42:1431–1442. https://doi.org/10.1111/jbi.12484
Tóth EG, Köbölkuti ZA, Pedryc A, Höhn M (2017) Evolutionary history and phylogeography of Scots pine (Pinus sylvestris L.) in Europe based on molecular markers. J Forest Res 28:637–651. https://doi.org/10.1007/s11676-017-0393-8
Tzedakis PC (2004) The Balkans as prime glacial refugial territory of European temperate trees. In: Griffiths HI, Kryštufek B, Reed JM (eds) Balkan biodiversity. Pattern and process in the European hotspot. Springer, Dordrecht, pp 49–68
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
Tzedakis PC, Emerson BC, Hewitt GM (2013) Cryptic or mystic? Glacial tree refugia in northern Europe. Trends Ecol Evol 28:696–704. https://doi.org/10.1016/j.tree.2013.09.001
van Andel TH, Tzedakis PC (1996) Palaeolithic landscapes of Europe and environs, 150,000–25,000 years ago: an overview. Quarten Sci Rev 15:481–500. https://doi.org/10.1016/0277-3791(96)00028-5
Williams MI, Dumroese RK (2013) Preparing for climate change: forestry and assisted migration. J Forest 111:287–297. https://doi.org/10.5849/jof.13-016
Willis KJ (1994) The vegetation history of the Balkans. Quarten Sci Rev 13:769–778. https://doi.org/10.1016/0277-3791(94)90104-X
Willis KJ, van Andel TH (2004) Trees or no trees? The environments of central and eastern Europe during the Last Glaciation. Quarten Sci Rev 23:2369–2387. https://doi.org/10.1016/j.quascirev.2004.06.002
Zanetto A, Roussel G, Kremer A (1994) Geographic variation of interspecific differentiation between Quercus robur L. and Quercus petraea (Matt.) Liebl. Forest Genet 1:111–123
Żukowska WB, Wachowiak W (2017) Nuclear microsatellite markers reveal the low genetic structure of Pinus mugo Turra (dwarf mountain pine) populations in Europe. Pl Syst Evol 303:641–651. https://doi.org/10.1007/s00606-017-1395-x
Acknowledgements
This study was supported by research grants of the Slovak Grant Agency for Science VEGA 1/0269/16 (DG), the National Science Fund of Bulgaria KP-06-H26/4 (PZ), and the Slovenian Research Agency research programme P4-0059 (RB).
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: Stanislav Španiel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gömöry, D., Zhelev, P. & Brus, R. The Balkans: a genetic hotspot but not a universal colonization source for trees. Plant Syst Evol 306, 5 (2020). https://doi.org/10.1007/s00606-020-01647-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-020-01647-x