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Ancient genetic bottleneck and Plio-Pleistocene climatic changes imprinted the phylobiogeography of European Black Pine populations

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Abstract

The historical changes in European Black Pine population size across the whole natural distribution in Europe and Asia Minor were analyzed facing the Plio-Pleistocene climatic fluctuations. Thirteen chloroplast SSRs and SNPs markers have been studied under the assumptions of “neutral evolution.” Populations and meta-populations had different histories of migration routes, and they were strongly affected by complex patterns of isolation, fragmentation, speciation, expansion (1.88–4.28 Ma), purification selection (2.09–21.41 Ma) and bottleneck (1.85–21.76 Ma). A significant number of populations (min. 29–41%) were in equilibrium for very long periods. Generally, the bottleneck revealed by chloroplast DNA is weaker than the bottleneck revealed by nuclear DNA. The N e immediately after the bottleneck reaches between 1820 and 3640 individuals. Generally, the historical effective population sizes shrink significantly for the Tertiary period from 10–15 up to 2.5 Ma in Western Europe (by 82%), followed by Asia Minor (69%) and the Balkan Peninsula (28%), likely resulting from important climatic changes. The rates and frequencies of stepwise westwards migration waves have been not sufficient to prevent isolation between the meta-populations and to suppress “sympatric speciation.” The migration was weak for the Pliocene, but was maximal for the Pleistocene, and finally silent for the present interglacial period, namely the Holocene.

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References

  • Akkemik U, Yılmaz H, Oral D et al (2010) Some changes in taxonomy of pines (Pinus L.) native to Turkey, Istanbul University. J Fac For 61(1):63–78

    Google Scholar 

  • Arslan M, Tosun S, Ok K et al. (2012) Seben Fosil Ormanı’nın Doğal ve Kültürel Değerlerinin Saptanması ve Uygun Yönetim Planının Geliştirilmesi (Determination of Natural and Cultural Values and Development of Management Plan in the Seben Petrified Forest), Batı Karadeniz Ormancılık Araştırma Enstitüsü Müdürlüğü (The Western Black Sea Forestry Research Institute), Press No: 31, ISBN 978-605-393-124-9

  • Bacles C, Jump A (2010) Taking a tree’s perspective on forest fragmentation genetics. Trends Plant Sci 16:13–18

    Article  PubMed  CAS  Google Scholar 

  • Bai W, Liao W, Zhang D (2010) Nuclear and chloroplast DNA phylogeography reveal two refuge areas with asymmetrical gene flow in a temperate walnut tree from East Asia. New Phytol 188:892–901

    Article  PubMed  Google Scholar 

  • Beaumont M (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beerli P (2006) Comparison of Bayesian and maximum likelihood inference of population genetic parameters. Bioinformatics 22:341–345

    Article  CAS  PubMed  Google Scholar 

  • Beerli P (2009) How to use MIGRATE or why are Markov chain Monte Carlo programs difficult to use? In: Bertorelle G, Bruford M, Hauffe H, Rizzoli A, Vernesi C (eds) Population genetics for animal conservation. Cambridge University Press, Cambridge. doi:10.1017/CBO9780511626920

    Google Scholar 

  • Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Belousov V, Volvovsky S, Arkhipov V et al (1988) Structure and evolution of the earth’s crust and upper mantle of the Black Sea Boll. Geofis Teor Appl 30:109–196

    Google Scholar 

  • Bijlsma R, Loeschcke V (2012) Genetic erosion impedes adaptive responses to stressful environments. Evol Appl 5:117–129

    Article  CAS  PubMed  Google Scholar 

  • Bogunic F, Yakovlev S, Muratovic E et al (2010) Different karyotype patterns among allopatric Pinus nigra (Pinaceae) populations revealed by molecular cytogenetics. Plant Biol 13(1):194–200

    Article  CAS  Google Scholar 

  • Bonavita S, Vendramin G, Bernardini V et al (2015) The first SSR-based assessment of genetic variation and structure among Pinus laricio Poiret populations within their native area. Plant Biosyst Int J Deal Asp Plant Biol. doi:10.1080/11263504.2015.1027316

    Google Scholar 

  • Braverman J, Hudson R, Kaplan N et al (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphism. Genetics 140:783–796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brooks A (2012) Phylogeography and Species distribution modeling of the flowering dogwood, Cornus florida L. (Cornaceae). Thesis. http://www.lib.ncsu.edu/resolver/1840.16/8880

  • Brown T (1997) Clearances and clearings: deforestation in mesolithic/neolithic britain. Oxf J Archaeol 16(2):133. doi:10.1111/1468-0092.00030

    Article  Google Scholar 

  • Bueno M, Pennington R, Dexter K et al (2016) Effects of quaternary climatic fluctuations on the distribution of neotropical savanna tree species. Ecography 39:001–012. doi:10.1111/ecog.01860

    Article  Google Scholar 

  • Cameron J, Williford A, Kliman R (2008) The Hill-Robertson effect: evolutionary consequences of weak selection in finite populations. Heredity 100:19–31

    Article  CAS  Google Scholar 

  • Campani M, Mulch A, Kempf O et al (2012) Miocene paleotopography of the Central Alps. Earth Planet Sci Lett 174:337–338. doi:10.1016/j.epsl.2012.05.017

    Google Scholar 

  • Carreras C, Pascual M, Cardona L et al (2007) The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications. Conserv Genet 8:761–775

    Article  CAS  Google Scholar 

  • Caujape-Castells J, Jansen R (2003) The influence of the Miocene Mediterranean desiccation on the geographical expansion and genetic variation of Androcymbium gramineum (Cav.) McBride (Colchicaceae). Mol Ecol 12:1515–1525

    Article  PubMed  Google Scholar 

  • Cengel B, Tayanc Y, Kandemir G et al (2012) Magnitude and efficiency of genetic diversity captured from seed stands of Pinus nigra (Arnold) subsp. pallasiana in established seed orchards and plantations. New For 43(3):303–317

    Article  Google Scholar 

  • Champagnac J, Schlunegger F, Norton K et al (2009) Erosion-driven uplift of the modern Central Alps. Tectonophysics 474(1–2):236–249. doi:10.1016/j.tecto.2009.02.024

    Article  Google Scholar 

  • Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205. doi:10.1038/nrg2526

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth J, Eyre-Walker A (2007) The other side of the nearly neutral theory, evidence of slightly advantageous back-mutations. Proc Natl Acad Sci USA 104:16992–16997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chetverikov S (1961) On certain aspects of the evolutionary process from the standpoint of modern genetics. (transl. of 1921 paper by Malina Parker; ed I.M. Lerner). Proc Am Philos Soc 105(2):167–195

    Google Scholar 

  • Christopoulou A, Fulé PZ, Andriopoulos P, Sarris D, Arianoutsou M (2013) Dendrochronology-based fire history of Pinus nigra forests in Mount Taygetos, Southern Greece. For Ecol Manage 293:132–139

    Article  Google Scholar 

  • Chybicki I, Dzialuk A (2014) Bayesian approach reveals confounding effects of population size and seasonality on outcrossing rates in a fragmented subalpine conifer. Tree Genet Genomes 10:1723–1737. doi:10.1007/s11295-014-0792-3

    Article  Google Scholar 

  • Clark C, Carbone I (2008) Chloroplast DNA phylogeography in long-lived Huon pine, a Tasmanian rain forest conifer. Can J For Res 38:1576–1589

    Article  CAS  Google Scholar 

  • Comps B, Gomory D, Letouzey J et al (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crow J, Morton N (1955) Measurement of gene frequency drift in small populations. Evolution 9:202–214

    Article  Google Scholar 

  • Davies S, Cavers S, Finegan B et al (2010) Genetic consequences of multigenerational and landscape colonisation bottlenecks for a neotropical forest pioneer tree, Vochysia ferruginea. Trop Plant Biol 3:14–27

    Article  CAS  Google Scholar 

  • Dijkstra S (1973) Fossilium catalogus.: II Plantae., Part 84, Alexander Doweld Publisher, ISBN: 9061933188, 9789061933182

  • Dobzhansky T (1982) Genetics and the origin of species, Reprint edn. Columbia University Press, New York

    Google Scholar 

  • Du Z-Y, Wang Q-F (2016) Allopatric divergence of Stuckenia filiformis (Potamogetonaceae) on the Qinghai-Tibet Plateau and its comparative phylogeography with S. pectinata in China. Sci. Rep. 6:20883. doi:10.1038/srep20883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eder J, Jechorek H, Kvacek Z et al (2008) The integrated plant record: an essential tool for reconstructing neogene zonal vegetation in Europe. Palaios 23:97–111. doi:10.2110/palo.2006.p06-039r

    Article  Google Scholar 

  • Edh K, Widen B, Ceplitis A (2007) Nuclear and chloroplast microsatellites reveal extreme population differentiation and limited gene flow in the Aegean endemic Brassica cretica (Brassicaceae). Mol Ecol 16:4972–4983

    Article  CAS  PubMed  Google Scholar 

  • Ehrendorfer F (2013) Woody plants—evolution and distribution since the tertiary: proceedings of a symposium organized by Deutsche Akademie der Naturforscher LEOPOLDINA in Halle/Saale, German Democratic Republic, 9–11 Oct 1986. Second publication In: Springer, 11 Nov 2013—Science

  • Excoffier L (2004a) Special issue: analytical methods in phylogeography and genetic structure. Mol Ecol 13:727. doi:10.1111/j.1365-294X.2004.02170.x

    Article  PubMed  Google Scholar 

  • Excoffier L (2004b) Analysis of population subdivision. Handbook of statistical genetics, vol 4. Wiley, p 24. doi:10.1002/0470022620.bbc25

  • Excoffier L, Schneider S, Roessli D (2002) Arlequin ver 2.001: a software for population genetics data analysis. Department of Anthropology and Ecology, University of Geneva, Geneva. http://cmpg.unibe.ch/software/arlequin/software/2.001/doc/whatsnew/whatsnew.html

  • Eyre-Walker A, Keightley P, Smith N et al (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol 19:2142–2149

    Article  CAS  PubMed  Google Scholar 

  • Fady-Welterlen B (2005) Is there really more biodiversity in Mediterranean forest ecosystems? Taxon 54:905–910

    Article  Google Scholar 

  • Finch J, Leng M, Marchant R (2009) Late quaternary vegetation dynamics in a biodiversity hotspot, the Uluguru Mountains of Tanzania. Quatern Res 72(1):111–122. doi:10.1016/j.yqres.2009.02.005

    Article  Google Scholar 

  • Flannery T (1994) The future eaters. Reed Books, Melbourne (ISBN: 0-7301-0422-2)

    Google Scholar 

  • Frantz L, Madsen O, Megens H et al (2014) Testing models of speciation from genome sequences: divergence and asymmetric admixture in Island South-East Asian Sus species during the Plio-Pleistocene climatic fluctuations. Mol Ecol 23(22):5566–5574. doi:10.1111/mec.12958

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu T (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaggiotti O, Excoffier L (2000) A simple method of removing the effect of a bottleneck and unequal population sizes on pairwise genetic distances. Proc R Soc Lond B 267:81–87

    Article  CAS  Google Scholar 

  • Galtier N, Depaulis F, Barton N (2000) Detecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics 155:981–987

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Y-D, Zhang Y, Gao X-F et al (2015) Pleistocene glaciations, demographic expansion and subsequent isolation promoted morphological heterogeneity: a phylogeographic study of the alpine Rosa sericea complex (Rosaceae). Sci Rep 5:11698. doi:10.1038/srep11698

    Article  PubMed  PubMed Central  Google Scholar 

  • Garza J, Williamson E (2001) Detection of reduction in population size using data from microsatellite DNA. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Geary D, Rich J, Valley J et al (1989) Stable isotopic evidence of salinity change: influence on the evolution of melanopsid gastropod in the late Miocene Pannonian basin. Geology 17:981–985

    Article  CAS  Google Scholar 

  • Goncharenko G, Silin A (1997) Populyatsionnaya i evolyutsionnaya genetika sosen Vostochnoi Evropy i Sibiri. [Population and Evolutionary Genetics of Pine in Eastern Europe and Siberia.] Tekhnalogiya, Minsk, Belarus (in Russian)

  • Gonzalez-Martınez S, Gerber S, Cervera M et al (2002) Seed gene flow and fine scale structure in a Mediterranean pine (Pinus pinaster Ait.) using nuclear microsatellite markers. Theor Appl Genet 104:1290–1297

    Article  PubMed  CAS  Google Scholar 

  • Gorbunov M (1958) Tretichnye sosny Zapadnoj Sibiri- Pinus thomasiana Varietas tomskiana and Pinus thomasiana Varietas kasparanica. Tomsk State University. Bot Z 3(43):349–350 (Russian)

    Google Scholar 

  • Gordo I, Navarro A, Charlesworth B (2002) Muller’s ratchet and the pattern of variation at a neutral locus. Genetics 161:835–848

    PubMed  PubMed Central  Google Scholar 

  • Gradstein F, Ogg J, Smith A et al (2005) A geologic time scale 2004. Cambridge University Press, Cambridge, 589 pp

    Book  Google Scholar 

  • Griffiths R, Tavare S (1994a) Simulating probability distributions in the coalescent. Theor Popul Biol 46:131–159

    Article  Google Scholar 

  • Griffiths R, Tavare S (1994b) Sampling theory for neutral alleles in a varying environment. Philos Trans R Soc Lond B Biol Sci 344:403–410

    Article  CAS  PubMed  Google Scholar 

  • Gulcu S, Ucler A (2008) Genetic variation of Anatolian black pine (Pinus nigra Arnold. subsp. pallasiana (Lamb.) Holmboe) in the Lakes district of Turkey. Silvae Genet 57:1–5

    Article  Google Scholar 

  • HAGRC-Helmholtz Association of German Research Centers (2009) Are the Alps growing or shrinking? Science Daily. www.sciencedaily.com/releases/2009/11/091105121207.htm

  • Hammor G, Halmai J (1988) Neogene paleogeographic atlas of central and Estern Europe. Geological Institute, Budapest

    Google Scholar 

  • Hampe A, Arroyo J, Jordano P et al (2003) Rangewide phylogeography of a bird-dispersed Eurasian shrub: contrasting Mediterranean and temperate glacial refugia. Mol Ecol 12:3415–3426

    Article  CAS  PubMed  Google Scholar 

  • Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66(4):591–600

    CAS  PubMed  Google Scholar 

  • Hartl D, Clark A (1997) Principles of population genetics, 3rd edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • He T, Pausas J, Belcher C et al (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol 194:751–759

    Article  PubMed  Google Scholar 

  • Heredia U, Nanos N, Rey E et al (2015) High seed dispersal ability of Pinus canariensis in stands of contrasting density inferred from genotypic data. For Syst 24(1):e-015. doi:10.5424/fs/2015241-06351

    Google Scholar 

  • Hofmann S, Kraus S, Dorge T et al (2014) Effects of Pleistocene climatic fluctuations on the phylogeography, demography and population structure of a high-elevation snake species, Thermophis baileyi, on the Tibetan Plateau. J Biogeogr 41:2162–2172. doi:10.1111/jbi.12358

    Article  Google Scholar 

  • Ivanov I (1971) Form variability of Pinus nigra (Arn.) in Western Rhodope Mountain. Ph.D. thesis, Forest Research Institute, Bulgarian Academy of Sciences, Sofia

  • Jipa D, Olariu C (2009) Dacian basin depositional architecture and sedimentary history of a Papatethys sea. National Institute of Marine Geology and Geo-Ecology (GeoEcoMar) - Romania, Special Publication No. 3

  • Juste J, Bilgin R, Munoz J et al (2009) Mitochondrial DNA signatures at different spatial scales: from the effects of the Straits of Gibraltar to population structure in the meridional serotine bat (Eptesicus isabellinus). Heredity 103:178–187

    Article  CAS  PubMed  Google Scholar 

  • Kamari S, Naydenov KD, Benyounes H et al (2010) Genetic signals of ancient decline in Aleppo pine populations at the species’ southwestern margins in the Mediterranean Basin. Hereditas 147:165–175. doi:10.1111/j.1601-5223.2010.02176.x

    Article  Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Kingman J (1982a) On the genealogy of large populations. In: Gani J, Hannan EJ (ed) Essays in statistical science. Applied Probability Trust, London, pp 27–43. (Also as J Appl Probab 19A: 27–43)

  • Kingman J (1982b) The coalescent. Stoch Process Appl 13:235–248

    Article  Google Scholar 

  • Kostov K (1974) One form of Pinus nigra (Arn.) very resistant to insects in Bulgaria. For Manag (Bulgaria) 3:6–16

    Google Scholar 

  • Kramer A, Ison A, Ashley M et al (2008) The paradox of forest fragmentation genetics. Conserv Biol 22:878–885

    Article  PubMed  Google Scholar 

  • Lee R, Daly R (1999) Cambridge encyclopedia of hunters and gatherers. Cambridge University Press, Cambridge, 534 pp

    Google Scholar 

  • Leys B, Finsinger W, Carcaillet C (2014) Historical range of fire frequency is not the Achilles’ heel of the Corsican black pine ecosystem. J Ecol 102:381–395

    Article  Google Scholar 

  • Li W (1977) Stochastic models in population genetics. Benchmark papers in genetics, vol 7. Dowden, Hutchinson & Ross, Stroudsburg, Pennsylvania. 484 S Biomed J 21: 297. doi:10.1002/bimj.4710210311

  • Lin H, Sanchez-Ortiz C, Hastings P (2009) Colour variation is incongruent with mitochondrial lineages: cryptic speciation and subsequent diversification in a Gulf of California reef fish (Teleostei: blennioidei). Mol Ecol 18:2476–2488

    Article  CAS  PubMed  Google Scholar 

  • Linares J, Tiscar P (2010) Climate change impacts and vulnerability of the southern populations of Pinus nigra subsp. salzmannii. Tree Physiol 30(7):795–806. doi:10.1093/treephys/tpq052

    Article  PubMed  Google Scholar 

  • Liu J, Möller M, Provan J et al (2013) Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot. New Phytol 199:1093–1108

    Article  PubMed  Google Scholar 

  • Lowe A (2005) Population genetics of neotropical trees focus issue. Heredity 95:243–245

    Article  CAS  PubMed  Google Scholar 

  • Lowe A, Boshier D, Ward M et al (2005) Genetic resource loss following habitat fragmentation and degradation; reconciling predicted theory with empirical evidence. Heredity 95:255–273

    Article  CAS  PubMed  Google Scholar 

  • Lumaret R, Mir C, Michaud H et al (2002) Phylogeographical variation of chloroplast DNA in holm oak (Quercus ilex L.). Mol Ecol 11:2327–2336

    Article  CAS  PubMed  Google Scholar 

  • Magyar I, Geary D, Muller P (1999) Paleogeographic evolution of the Late Miocene Lake Pannon in Central Europe. Palaeogeogr Palaeoclimatol Palaeoecol 147:151–167

    Article  Google Scholar 

  • Mann H, Whitney D (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18(1):50–60. doi:10.1214/aoms/1177730491

    Article  Google Scholar 

  • Marshall H, Newton C, Ritland K (2002) Chloroplast phylogeography and evolution of highly polymorphic microsatellites in lodgepole pine (Pinus contorta). Theor Appl Genet 104:367–387

    Article  CAS  Google Scholar 

  • Mihailov V (1983) Sur la variabilite´ endoge`ne des aiguilles et son importance pour la taxonomie du pin noir (Pinus nigra Arn.). For Sci (Bulgaria) 1:3–20

    Google Scholar 

  • Mihailov V (1987) Variability of European Black pine (Pinus nigra Arn.) in size, weight and form of the seeds in Pirin and Slavianka mountains. For Sci (Bulgaria) 6:26–37

    Google Scholar 

  • Mihailov V (1993) Biological and morphological study of the European Black pine’s (Pinus nigra Arn.) seeds in different provenances and selection structure in Pirin and Slavianka mountains in Bulgaria. Ph.D. thesis, Forest Research Institute, Bulgarian Academy of Sciences, (Bulgaria), Sofia

  • Mihailov V (1998) Variability of European Black pine (Pinus nigra Arn.) according to the size, weight and form of the apophysis of the cones in Pirin and Slavianka mountains. For Sci (Bulgaria) 1(2):24–37

    Google Scholar 

  • Milankovitch M (1920) Theorie Mathematique des Phenomenes Thermiques produits par la Radiation Solaire. Gauthier-Villars et Cie., Paris, 338 pp

    Google Scholar 

  • Milankovitch M (1930) Mathematische Klimalehre und Astronomische Theorie der Klimaschwankungen, Handbuch der Klimalogie Band 1 Teil A Borntrager Berlin

  • Milankovitch M (1941) Canon of Insolation and the ice age problem. Zavod za Udz̆benike i Nastavna Sredstva, Belgrade. ISBN: 86-17-06619-9

  • Mirov N (1967) The genus Pinus. The Ronald Press, New York, p 610

    Google Scholar 

  • Moores E, Fairbridge R (1998) Encyclopedia of European and Asian regional geology. Encyclopedia of Earth Sciences Series, London

    Google Scholar 

  • Naydenov KD, Alexandrov A (1999) Geographic variability of some of the Monoterpines (α-pinene, camphene and β-pinene) in Authohtonious population of Scots Pine (Pinus sylvestris L.) in Rila-Rhodopses massif. Diagnosis Press. J Biotechnol Biotechnol Equip 13(2):14–18

    Article  CAS  Google Scholar 

  • Naydenov KD, Alexandrov A (2000) Application of transformed data on terpenes in Pinus sylvestris L. populations for phenotypic studies. Diagnosis Press. J Biotechnol Biotechnol Equip 14(1):40–46

    Article  CAS  Google Scholar 

  • Naydenov KD, Alexandrov A, Tremblay F (2002) Terpene composition of Scots pine (Pinus sylvestris L.) in the eastern part of the Balkan Peninsula. 1. Provenance tests. Diagnosis Press. J Biotechnol Biotechnol Equip 16(2):99–108

    CAS  Google Scholar 

  • Naydenov KD, Tremblay F, Bergeron Y et al (2006) Germination response to forest fire-related charcoal active effect of Jack pine (Pinus banksiana Lamb.) seeds. Can J For Res 36:761–767

    Article  Google Scholar 

  • Naydenov KD, Naydenov MK, Tremblay F et al (2011) Patterns of genetic diversity that result from bottlenecks in Scots Pine and the implications for local genetic conservation and management practices in Bulgaria. New For 42:179–193. doi:10.1007/s11056-010-9245-5

    Article  Google Scholar 

  • Naydenov KD, Alexandrov A, Naydenov M et al (2012) Impact of activated charcoal on germination and initial growth of some pine species. J Balk Ecol 15(3):277–293

    Google Scholar 

  • Naydenov KD, Alexandrov A, Matevski V et al (2014) Range-wide genetic structure of maritime pine predates the last glacial maximum: evidence from nuclear DNA. Hereditas 151:1–13. doi:10.1111/j.1601-5223.2013.00027.x

    Article  PubMed  Google Scholar 

  • Naydenov KD, Mladenov I, Alexandrov A et al (2015) Patterns of genetic diversity resulting from bottlenecks in European black pine, with implications on local genetic conservation and management practices in Bulgaria. Eur J For Res 134(4):669–681. doi:10.1007/s10342-015-0881-3

    Article  Google Scholar 

  • Naydenov KD, Naydenov MK, Alexandrov A et al (2016) Ancient split of major genetic lineages of European black pine: evidence from chloroplast DNA. Tree Genet Genomes 12(68):1–18. doi:10.1007/s11295-016-1022-y

    Google Scholar 

  • NordNordWest Trust-Germany (2005) exhibition—Ausstellung “Meeresstrand am Alpenrand” der Niederösterreichischen Landesmuseum, under licence. http://creativecommons.org/licenses/by-sa/3.0/de/legalcode, ISBN: 978-3-85252-644-7

  • Overpeck J, Otto-Bliesner B, Miller G et al (2006) Paleoclimatic evidence for future ice-sheet instability and rapid sea-level rise. Science 311(5768):1747–1750. doi:10.1126/science.1115159

    Article  CAS  PubMed  Google Scholar 

  • Paape T, Igic B, Smith S et al (2008) A 15-Myr-old genetic bottleneck. Mol Biol Evol 25(4):655–663. doi:10.1093/molbev/msn016

    Article  CAS  PubMed  Google Scholar 

  • Palamarev E (1989) Paleobotanical evidences of the tertiary history and origin of the Mediterranean sclerophyll dendroflora. Plant Syst Evol 162(1/4):93–107

    Article  Google Scholar 

  • Papaianopol I, Marinescu F, Popescu A et al (1987) Paleogeographie du Pontien du Bassin Dacique, insistant sur le developement du facies charboneux. D S Inst Geol Geofiz Bucarest 72–73(4):261–275

    Google Scholar 

  • Petit R, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214

    Article  Google Scholar 

  • Petit R, Hampe A, Cheddadi R (2005) Climate changes and tree phylogeography in the Mediterranean. Taxon 54(4):877–885

    Article  Google Scholar 

  • Popov S, Rogl F, Rozanov A et al (2004) Lithological paleogeographic maps of Paratethys. 10 maps Late Eocene to Pliocene. Cour Forsch Senckenberg 250:1–46

    Google Scholar 

  • Poulsen T, Veyret P, Diem A (2015) The Alps. Encyclopedia Britannica

  • Rafii Z, Dodd R (2007) Chloroplast DNA supports a hypothesis of glacial refugia over post-glacial recolonization in disjunct populations of black pine (Pinus nigra) in Western Europe. Mol Ecol 16:723–736

    Article  CAS  Google Scholar 

  • Richmond G, Fullerton D (1986) Summation of quaternary glaciations in the United States of America. Quatern Sci Rev 5:183–196. doi:10.1016/0277-3791(86)90184-8

    Article  Google Scholar 

  • Rogers A (1995) Genetic evidence for a pleistocene population explosion. Evolution 49(4):608–615. doi:10.2307/2410314

    Article  PubMed  Google Scholar 

  • Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Rozas J, Sanchez-Del-Barrio J, Messeguer X et al (2003) Dna SP, DNA polymorphism analysis by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Rubio-Moraga A, Candel-Perez D, Lucas-Borja M et al (2012) Genetic diversity of Pinus nigra Arn. populations in southern Spain and northern Morocco revealed By inter-simple sequence repeat profiles. Int J Mol Sci 13:5645–5658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saulea E, Popescu I, Săndulescu J (1969) Atlas litofacial. VI – Neogen, 1:200.000 (in Romanian and in French). Institute Geologic, Bucureşti

    Google Scholar 

  • Savolainen O, Pyhajarvi T, Knurr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol S 38:595–619

    Article  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152(3):1079–1089

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scotese C (2001) Atlas of earth history. PALEOMAP Project, Arlington, p 52

    Google Scholar 

  • Scotese C, Golonka J (1992) PALEOMAP paleogeographic Atlas, PALEOMAP Progress Report No. 20. Department of Geology, University of Texas at Arlington, Arlington

    Google Scholar 

  • Scotese C, Kazmin V, Natapov L et al (1998) The paleogeographic atlas of northern Eurasia. Institute of Tectonics of Lithospheric Plates, Russian Academy of Sciences, Moscow (26 maps)

    Google Scholar 

  • Sengor A, Natalin B (1996) Palaeotectonics of Asia: fragments of a synthesis, the tectonic evolution of Asia. In: Yin A, Harrison M (eds) Rubey Colloquium. Cambridge University Press, Cambridge, pp 486–640

    Google Scholar 

  • SGN-Senckenberg Research Institute and Natural History Museum (2012) Outstanding for the past 15 million years: swiss Alps have influenced Europe’s climate since the Miocene. Science Daily. www.sciencedaily.com/releases/2012/07/120710093407.htm

  • Shapiro S, Wilk M (1965) An analysis of variance test for normality. Biometrika 52(3–4):591–611. doi:10.1093/biomet/52.3-4.591

    Article  Google Scholar 

  • Simonsen K, Churchill G, Aquadro C (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413–429

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sivacioglu A, Ayan S (2010) Variation in cone and seed characteristics in a clonal seed orchard of Anatolian black pine [Pinus nigra Arnold subsp. pallasiana (Lamb.) Holmboe]. J Environ Biol 31:119–123

    CAS  PubMed  Google Scholar 

  • Stebbins G (1974) Flowering plants. Evolution above the species level. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Stefanov B (1941/1942) Geographical distribution of coniferous species and their form in nature, vols XIX–XX. Godichnik na Sofiiskia Darjaven Universitet, Sofia

  • Stefanov B (1943) The phyto-geographical elements of Bulgaria. Thesis of Bulgarian Academy of Sciences, Faculty of Nature and Mathematics, Sofia, vol. XXXIX, N 19

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor D, Keller S (2007). Historical range expansion determines the phylogenetic diversity introduced during contemporary species invasion. Evolution 61(2): 334–345. http://www.jstor.org/stable/4621290

  • Thesing B, Noye R, Starkey D et al (2016) Pleistocene climatic fluctuations explain the disjunct distribution and complex phylogeographic structure of the southern red-backed Salamander, Plethodon serratus. Evol Ecol 30:89. doi:10.1007/s10682-015-9794-3

    Article  Google Scholar 

  • Vendramin G, Lelli L, Rossi P et al (1996) A set of primer for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5:585–598

    Article  Google Scholar 

  • Vidakovic M (1991) Conifers: morphology and variation. Graficki Zavod Hrvatske, Croatia

    Google Scholar 

  • Wakeley J, Aliacar N (2001) Gene genealogies in a meta-population. Genetics 159:893–905

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Wu Y, Ren G et al (2011) Genetic differentiation and delimitation between ecologically diverged Populus euphratica and P. pruinosa. PLOS ONE 6(10):e26530. doi:10.1371/journal.pone.0026530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woolfit M, Bromham L (2005) Population size and molecular evolution on islands. Proc R Soc B 272:2277–2282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright S (1938) Size of population and breeding structure in relation to evolution. Science 87:430–431

    Google Scholar 

  • Wright S (1942) Statistical genetics and evolution. Bull Am Math Soc 48(4):223–246. doi:10.1090/S0002-9904-1942-07641-5

    Article  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations, vol 2. University Chicago Press, Chicago

    Google Scholar 

  • Yuan Z-Y, Suwannapoom C, Yan F et al (2016) Red River barrier and Pleistocene climatic fluctuations shaped the genetic structure of Microhyla fissipes complex (Anura: Microhylidae) in southern China and Indochina. Curr Zool 62(6):531–543. doi:10.1093/cz/zow042

    Article  Google Scholar 

  • Ziegler P (1988) Evolution of the Arctic-North Atlantic and the western Tethys. AAPG Memoir 43:164–196

    Google Scholar 

Download references

Acknowledgements

We would like to thank Irena M. Naydenova, T&T for their technical assistance; the two anonymous organizations for their financial support; Ph.D. Z. Kaya (Turkey), Ph.D. M. Kostadinovski (Macedonia), M. Topac (Turkey) and Ph.D. C. Varelides (Greece), who all made direct (and indirect) logistical help in supplying some samples. We would also like to thank the Ministers of Forestry, Education and Science of all the countries with participant persons for providing the funding for sample collection and fruitful collaboration. We also wish to thank the Nature Publishing Group Language Editing-NPGLE (www.languageediting.nature.com) for the careful English revision of this manuscript.

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Authors and Affiliations

  1. Ministry of National Defence - CAF, 25 Grand-Bernier, St-Jean-sur-Richelieu, QC, J0J1R0, Canada

    Krassimir D. Naydenov

  2. Faculty of Medicine, Ss. Cyril and Methodius University, 50 Divizija 6, 1000, Skopje, Republic of Macedonia

    Michel K. Naydenov

  3. Bulgarian Academy of Science, Forest Research Institute, 132 Bd. Kliment Ochridskii, 1756, Sofia, Bulgaria

    Alexander Alexandrov, Georgi Hinkov & Veselka Gyuleva

  4. Faculty of Forestry, Ss. Cyril and Methodius University, Blvd. Edvard Kardelj bb, 1000, Skopje, Republic of Macedonia

    Kole Vasilevski

  5. Faculty of Natural Sciences and Mathematics, Institute of Biologie, 1000, Skopje, Republic of Macedonia

    Vlado Matevski

  6. Institute of Forestry, Kneza Višeslava 3, Belgrade, 11000, Serbia

    Biljana Nikolic

  7. Forest Ecology and Forest Management, Wageningen University, P.O. Box 47, 6700 AA, Wageningen, The Netherlands

    Venceslas Goudiaby

  8. Department of Mathematics and Statistics, Queen’s University, Jeffery Hall, University Ave., Kingston, ON, K7L 3N6, Canada

    Dave Riegert

  9. Ministry of Reconstruction of Production, Environment, and Energy, 31 Xalkokondili, 10164, Athens, Greece

    Despina Paitaridou

  10. Departament of Forestry, 26 Loukis Akritas Avenue, 1414, Nicosia, Cyprus

    Andreas Christou

  11. Faculty of Biology and Geology, Babes-Bolyai University, Republicii Street 42, 400015, Cluj-Napoca, Romania

    Irina Goia

  12. Ecole Pratique des Hautes Etudes PSLResearch University Paris, Paris, France

    Christopher Carcaillet

  13. LEHNA (UMR5023) CNRS, Université Lyon 1, 43 Bd 11 Novembre 1918, 69622, Villeurbanne Cedex, France

    Christopher Carcaillet

  14. Area de Biodiversidad and Conservacion, Universidad Rey Juan Carlos, Tulipan, 28933, Mostoles, Madrid, Spain

    Adrian Escudero Alcantara

  15. Department of Biology, Ecology Program, Science Faculty, Anadolu University, 26470, Eskisehir, Turkey

    Cengiz Ture

  16. Forestry Faculty, Suleyman Demirel University, 32260, Isparta, Turkey

    Suleyman Gulcu

  17. Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bul. Despota Stefana 142, Belgrade, Serbia

    Srdjan Bojovic

  18. Dipartimento di Biologia, Università di Pisa, 56126, Pisa, Italy

    Lorenzo Peruzzi

  19. Faculté des Sciences, Université Mohamed Premier, Oujda, 63, rue Al maqdis Alqods, 60000, Oujda, Morocco

    Salim Kamary

  20. Petrozavodsk State University, Petrozavodsk, Lenin Avenue 33, Petrozavodsk, Republic of Karelia, Russia, 185910

    Anatoly Tsarev

  21. Faculty of Forestry, University of Sarajevo, 20 Zagrebacka, Sarajevo, Bosnia and Herzegovina

    Faruk Bogunic

Authors
  1. Krassimir D. Naydenov
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  2. Michel K. Naydenov
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  3. Alexander Alexandrov
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  19. Lorenzo Peruzzi
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  22. Faruk Bogunic
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Corresponding author

Correspondence to Krassimir D. Naydenov.

Additional information

Communicated by Rüdiger Grote.

This article is dedicated to the memory of Prof. Dr. Dimitar Velkov from Forest Research Institute, Bulgarian Academy of Science (1921–2001).

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Naydenov, K.D., Naydenov, M.K., Alexandrov, A. et al. Ancient genetic bottleneck and Plio-Pleistocene climatic changes imprinted the phylobiogeography of European Black Pine populations. Eur J Forest Res 136, 767–786 (2017). https://doi.org/10.1007/s10342-017-1069-9

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  • DOI: https://doi.org/10.1007/s10342-017-1069-9

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