Skip to main content

Advertisement

SpringerLink
Log in

Ancient split of major genetic lineages of European Black Pine: evidence from chloroplast DNA

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

The European Black Pine (Pinus nigra Arn.) has a long and complex history. Genetic distance and frequency analyses identified three differentiated genetic groups, which corresponded to three wide geographical areas: Westerns Mediterranean, Balkan Peninsula and Asia Minor. These groups shared common ancestors (14.75 and 10.72 Ma). The most recent splits occurred after the Messinian Salinity Crisis (4.37 Ma) and the Early–Middle Pleistocene Transitions (0.93 Ma). The posterior ancestral population size (Na) is 260,000–265,000 individuals. Each pool is further fragmented, with evidence of a phylogeographic structure (N st  > G st ) typically observed in some natural populations from the Western Mediterranean region and the Balkan Peninsula. The laboratory analysis was performed by fragment analysis—i.e. electrophoretic sizing of polymerase chain reaction fragments, combined with the sequencing analysis of 33 % of all individuals as a control. Intense sampling of chloroplast DNA polymorphisms (3154 individuals and 13 markers: SNPs and SSRs) over the full area of the species’ natural distribution indicated moderate among-population variability (G st(nc) ≤ 0.177) in various parts of its range. These results indicate that the natural populations have long migration histories that differ from one another and that they have been strongly phylogeographically affected by complex patterns of isolation, speciation and fragmentation. Long and varying climatic fluctuations in the region of the principal genetic group have been the probable cause of different forest community associations with different successional patterns resulting in interglacial refugia vs. macro long-term refugia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams RI, Brown KM, Hamilton MB (2004) The impact of microsatellite electromorph size homoplasy on multilocus population structure estimates in a tropical tree (Corythophora alta) and an anadromous fish (Morone saxatilis). Mol Ecol 13(9):2579–2588

    Article  CAS  PubMed  Google Scholar 

  • Balaresque P, Bowden GR, Adams SM, et al. (2010) A predominantly Neolithic origin for European paternal lineages. PLoS Biol 8(1):e1000285. doi:10.1371/journal.pbio.1000285

    Article  PubMed  PubMed Central  Google Scholar 

  • Belkhir K (2000) Genetix ver 4.01: a software for population genetics data analysis. Loboratoire genome et populations. Universite de Montpellier, II, France

    Google Scholar 

  • Bojović S (1995) Biodiversité du pin noir (Pinus nigra Arn.) en région méditerranéenne. Thèse doctorale. Université d’Aix-Marseille III, France, pp. 1–114

    Google Scholar 

  • Bonavita S, Vendramin GG, 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 Dealing Asp Plant Biol. doi:10.1080/11263504.2015.1027316

    Google Scholar 

  • Bucci G, Gonzalez-Martinez SC, Le Provost G, et al. (2007) Range-wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers. Mol Ecol 16(10):2137–2153. doi:10.1111/j.1365-294X.2007.03275.x

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Durand E, Forbes F, et al. (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756

    Article  Google Scholar 

  • Cinget B, Gérardi S, Beaulieu J, et al. (2015) Less pollen-mediated gene flow for more signatures of glacial lineages: congruent evidence from Balsam Fir cpDNA and mtDNA for multiple refugia in eastern and Central North America. PLoS One 10(4):e0122815. doi:10.1371/journal.pone.0122815

    Article  PubMed  PubMed Central  Google Scholar 

  • Coart E, Van Labeke S, De Loose M, et al. (2006) Chloroplast diversity in the genus Malus: new insights into the relationship between the European wild apple (Malus sylvestris (L.) Mill.) and the domesticated apple (Malus domestica Borkh.). Mol Ecol 15:2171–2182. doi:10.1111/j.1365-294X.2006.02924.x

    Article  CAS  PubMed  Google Scholar 

  • Critchfield WB, Little EL (1966) Geographic distribution of the pines of the world. U.S.D.A. Forest Service Miscellaneous Publication 991

  • Delplancke M, Alvarez N, Espíndola A, et al. (2012) Gene flow among wild and domesticated almond species: insights from chloroplast and nuclear markers. Evol Appl 5:317–329. doi:10.1111/j.1752-4571.2011.00223.x

    Article  CAS  PubMed  Google Scholar 

  • Dobrinov I, Doykov G, Gagov V (1982) Forest genetic pool in Bulgaria. Zemizdat, Sofia [in Bulgarian]--

    Google Scholar 

  • Doyle JJ, Morgante M, Tingey SV, et al. (1998) Size homoplasy in chloroplast microsatellites of wild perennial relatives of soybean (Glycine subgenus glycine). Mol Biol Evol 15(2):215–218

    Article  CAS  PubMed  Google Scholar 

  • Duminil J, Heuertz M, Doucet J-L, et al. (2010) CpDNA-based species identification and phylogeography: application to African tropical tree species. Mol Ecol 19:5469–5483. doi:10.1111/j.1365-294X.2010.04917.x

    Article  CAS  PubMed  Google Scholar 

  • Dzialuk A, Muchewicz E, Boratynski A, et al. (2009) Genetic variation of Pinus uncinata (Pinaceae) in the Pyrenees determined with cpSSR markers. Plant Syst Evol 277:197–205. doi:10.1007/s00606-008-0123-y

    Article  CAS  Google Scholar 

  • Eckenwalder JE (2009) Conifers of the world—the complete reference. Timber Press, Oregon, 720p

  • Emerson BC, Hewitt GM (2005) Phylogeography. Curr Biol 15(10):R367–R371

    Article  CAS  PubMed  Google Scholar 

  • Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

  • Evanno G, Regnau S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  • 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, Switzerland

    Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003a) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Falush D, Wirth T, Linz B, et al. (2003b) Traces of human migrations in Helicobacter pylori populations. Science 299:1582–1585

    Article  CAS  PubMed  Google Scholar 

  • Farjon A (2008) A natural history of conifer. Timber Press, Oregon, 304p

  • Fineschi S (1984) Determination of the origin of an isolated group of trees of Pinus nigra through enzyme gene markers. Silvae Genet 33:169–172

    Google Scholar 

  • François O, Ancelet S, Guillot G (2006) Bayesian clustering using hidden Markov random fields in spatial population genetics. Genetics 174:805–816

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukarek P (1958a) Prilog poznavanju crnog bora (Pinus nigra ARN. S. lat.) Beitrag zur Kenntnis der systematischen Stellung, Gliederung und der rezenten Verbreitung der Schwarzkiefer. Rad Poljopr Sumersk Fak Univ Sarajevu 3:3–92 [in German]

    Google Scholar 

  • Fukarek P (1958b) Standortrassen der Schwarzfhre (Pinus nigra ARN. S. lat.). Centralbl Gesamten Forstwes 75:203–207 [in German]

    Google Scholar 

  • García-Amorena I, Rubiales JM, Amat EM, et al. (2011) New macrofossil evidence of Pinus nigra Arnold on the northern Iberian Meseta during the Holocene. Rev Palaeobot Palynol 63(3–4):281–288. doi:10.1016/j.revpalbo.2010.10.010

    Article  Google Scholar 

  • Gealey WK (1989) Plate tectonic evolution of the Mediterranean ’ Middle East region. In: Scotese CR, Sager WW (eds) Mesozoic and Cenozoic plate reconstructions. Elsevier, Amsterdam, pp. 285–306

    Google Scholar 

  • Godbout J, Fazekas A, Newton CH, et al. (2008) Glacial vicariance in the Pacific northwest: evidence from a lodgepole pine mitochondrial DNA minisatellite for multiple genetically distinct and widely separated refugia. Mol Ecol 17(10):2449–2462. doi:10.1111/j.1365-294X.2008.03761.x

    Article  Google Scholar 

  • Gomez A, Aguiriano E, Alía R, et al. (2002) Análisis de los recursos genéticos de Pinus pinea L. en España mediante microsatélites del cloroplasto. Invest Agr Sist Recur For 11(1):145–154 [in Spanisch]

    Google Scholar 

  • Gomez A, Vendramin GG, González-Martínez SC, et al. (2005) Genetic diversity and differentiation of two Mediterranean pines (Pinus halepensis Mill. and Pinus pinaster Ait.) along a latitudinal cline using chloroplast microsatellite markers. Divers Distrib 11:257–263

    Article  Google Scholar 

  • Grant V (1980) Gene flow and the homogeneity of species populations. Biol Zbl 99:157–169

    Google Scholar 

  • Grivet D, Petit RJ (2003) Chloroplast DNA phylogeography of the hornbeam in Europe: evidence for a bottleneck at the outset of postglacial colonization. Conserv Genet 4:47–56

    Article  CAS  Google Scholar 

  • Hale ML, Borland AM, Gustafsson MHG, et al. (2004) Causes of size homoplasy among chloroplast microsatellites in closely related Clusia species. J Mol Evol 58:182–190

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. doi:10.1046/j.1471-8278.2002.00305.x

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Heuertz M, Carnevale S, Fineschi S, et al. (2006) Chloroplast DNA phylogeography of three European ashes, Fraxinus sp. (Oleaceae): roles of hybridization and contrasting mating systems. Mol Ecol 15:2131–2140

    Article  CAS  PubMed  Google Scholar 

  • Heuertz M, Teufel J, González-Martínez SC, et al. (2010) Geography determines genetic relationships between species of mountain pine (Pinus mugo complex) in Western Europe. J Biogeogr 37(3):541–556. doi:10.1111/j.1365-2699.2009.02223.x

    Article  Google Scholar 

  • Hodel RG, Gonzales E (2013) Phylogeography of sea oats (Uniola paniculata), a dune-building coastal grass in Southeastern North America. J Hered, June, doi:10.1093/jhered/est035

  • Hohn M, Gugerli F, Abran P, et al. (2009) Variation in the chloroplast DNA of Swiss stone pine (Pinus cembra L.) reflects contrasting post-glacial history of populations from the Carpathians and the Alps. J Biogeogr. doi:10.1111/j.1365-2699.2009.02122.x

    Google Scholar 

  • Hudson RR (1990) Gene genealogies and the coalescent process. Oxf Surv Evol Biol 7:1–44

    Google Scholar 

  • Iversen J (1973) The development of Denmark’s nature since the last glacial. Dan Geol Undersogelse 7C:1–126

    Google Scholar 

  • Jaramillo-Correa JP, Aguirre-Planter E, Khasa DP, et al. (2008) Ancestry and divergence of subtropical montane forest isolates: molecular biogeography of the genus Abies (Pinaceae) in southern Mexico and Guatemala. Mol Ecol 17(10):2476–2490. doi:10.1111/j.1365-294X.2008.03762.x

    Article  CAS  PubMed  Google Scholar 

  • Joos F, Colin PI (2004) A paleo-perspective on changes in atmospheric CO2 and climate. The global carbon cycle: integrating humans, climate, and the natural world. Scope 62:165–186

    CAS  Google Scholar 

  • Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kalinowski ST (2009) How well do evolutionary trees describe genetic relationships between populations? Heredity 102:506–513

    Article  CAS  PubMed  Google Scholar 

  • Kayser M, Brauer S, Cordaux R, et al. (2006) Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific. Mol Biol Evol 23(11):2234–2244

    Article  CAS  PubMed  Google Scholar 

  • Kingman JFC (1982) The coalescent. Stoch Process Appl 13(3):235–248. doi:10.1016/0304-4149(82)90011-4

    Article  Google Scholar 

  • Lande R, Engen S, Saether BE (1999) Spatial scale of population synchrony: environmental correlation vs. dispersal and density regulation. Am Nat 154:271–281

    Article  PubMed  Google Scholar 

  • Lande R, Engen S, Saether BE (2003) Stochastic population dynamics in ecology and conservation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Lehman N (1998) Conservation biology: genes are not enough. Curr Biol 8:R722–R724

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    Article  CAS  PubMed  Google Scholar 

  • Lumaret R, López de Heredia U, Soto A (2009) Origin and genetic variability of cork-oak. In: Aronson J, Pereira JS, Pausas J (eds) Cork oak woodlands on the edge: ecology, adaptive management and restoration. Island Press, Washington, DC, pp. 25–32

    Google Scholar 

  • Lumaret R, Tryphon-Dionnet M, Michaud H, et al. (2005) Phylogeographical variation of chloroplast DNA in cork oak (Quercus suber). Ann Bot 96:853–861. doi:10.1093/aob/mci237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190

    Article  PubMed  Google Scholar 

  • Maslin MA, Ridgwell AJ (2005) Mid-Pleistocene revolution and the ‘eccentricity myth’. In: Head, M.J., Gibbard, P.L. (Ed), “Early–Middle Pleistocene transitions: the land–ocean evidence”, Geol Soc Lond, Spec Publ, 247: 19–34.

  • Miller P (1768) The gardeners dictionary. Ed. 8. London

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

  • Navascués M, Emerson BC (2005) Chloroplast microsatellites: measures of genetic diversity and the effect of homoplasy. Mol Ecol 14:1333–1341. doi:10.1111/j.1365-294X.2005.02504.x

  • 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, 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(2):179

    Article  Google Scholar 

  • Naydenov KD, Senneville S, Beaulieu J, et al. (2007) Glacial vicariance in Eurasia: mitochondrial DNA evidence from Scots Pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor. BMC Evol Biol 7:233. doi:10.1186/1471-2148-7-233

    Article  PubMed  PubMed Central  Google Scholar 

  • Naydenov KD, Tremblay F, Fenton N (2005) Chloroplast microsatellites analysis revealed a high level of differentiation in Jack pine (Pinus banksiana Lamb.) population in Quebec. Belg J Bot 138(2):181–191

    Google Scholar 

  • Naydenov KD, Tremblay F, Fenton NJ, et al. (2006) Structure of Pinus nigra Arn. populations in Bulgaria revealed by chloroplast microsatellites and terpenes analysis: provenance tests. Biochem Syst Ecol 34:562–574

    Article  CAS  Google Scholar 

  • Naydenov KD, Tremblay F, Ganchev P (2003) Karyotype diversity in of European Black Pine (Pinus nigra Arn.) from Bulgarian provenances. Phyton 43(1):9–28

    Google Scholar 

  • Nei M, Chesser RK (1983) Estimation of fixation indices and gene diversities. Ann Hum Genet 47:253–259

    Article  CAS  PubMed  Google Scholar 

  • Palamarev E (1989) Paleobotanical evidences of the Tertiary history and origin of the Mediterranean sclerophyll dendroflora. Woody plants—evolution and distribution since the Tertiary. Plant Syst Evol 162(1/4):93–107

    Article  Google Scholar 

  • Perdereau AC, Kelleher CT, Douglas GC, Hodkinson TR (2014) High levels of gene flow and genetic diversity in Irish populations of Salix caprea L. inferred from chloroplast and nuclear SSR markers. BMC Plant Biol 14:202. doi:10.1186/s12870-014-0202-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu J-L, et al. (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300(5625):1563. doi:10.1126/science.1083264

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, Brewer S, Bordaes S, et al. (2002a) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manag 156:49–74

    Article  Google Scholar 

  • Petit RJ, Csaikl UM, Bordaes S, et al. (2002b) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2,600 populations. For Ecol Manag 156:5–26

    Article  Google Scholar 

  • Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24(7):386–393

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Pianka ER (1978) Evolutionary ecology. Harper and Row, New York

    Google Scholar 

  • Pico FX, Mendez-Vigo B, Martinez-Zapater JM, et al. (2008) Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian Peninsula. Genetics 180(2):1009–1021. doi:10.1534/genetics.108.089581

    Article  PubMed  PubMed Central  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powell W, Morgante M, Andre C, et al. (1995b) Hypervariable microsatellites provide a general source of polymorphic DNA markers for the chloroplast genome. Curr Biol 5:1023–1029

    Article  CAS  PubMed  Google Scholar 

  • Powell W, Morgante M, McDevitt R, et al. (1995a) Polymorphic simple sequence repeat regions in the chloroplast genome: applications to the population genetics of pines. Proc Natl Acad Sci U S A 92:7759–7763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

  • Pritchard JK, Wen W (2003) Documentation for structure software Version 2 [online]. Available from http://pritch.bsd.uchicago.edu/software/readme_2_1/readme.html

  • Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23(10):564–571. doi:10.1016/j.tree.2008.06.010

  • Provan J, Soranzo N, Wilson NJ, et al. (1999) A low mutation rate for chloroplast microsatellites. Genetics 153:943–947

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raffi ZA, Dodd RS (2007) Chloroplast DNA supports a hypothesis of glacial refugia over postglacial recolonization in disjunct populations of black pine (Pinus nigra) in Western Europe. Mol Ecol 16(4):723–736

    Article  Google Scholar 

  • Raufaste N, Bonhomme F (2000) Properties of bias and variance of two multiallelic estimators of Fst. Theor Popul Biol 57:285–296

    Article  CAS  PubMed  Google Scholar 

  • Robertson A, Hill WG (1984) Deviations from Hardy-Weinberg proportions: sampling variances and use in estimation of inbreeding coefficients. Genetics 107:703–718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers JS (1972) Measures of similarity and genetic distance. In studies in genetics VII. University of Texas Publication 7213, Austin, Texas, p 145−153

  • Roiron P, Chabal L, Sueiral I, et al. (2013) Palaeobiogeography of Pinus nigra Arn. subsp. salzmannii (Dunal) Franco in the north-western Mediterranean Basin: a review based on macroremains. Rev Palaeobot Palynol 194:1–11. doi:10.1016/j.revpalbo.2013.03.002

  • Scotti I, Paglia G, Magni F, et al. (2006) Population genetics of Norway spruce (Picea abies Karst.) at regional scale: sensitivity of different microsatellite motif classes in detecting differentiation. Ann For Sci 63:485–491. doi:10.1051/forest:2006029

    Article  CAS  Google Scholar 

  • Semerikov VL, Semerikova SA, Dymshakova OS, et al. (2014) Microsatellite loci polymorphism of chloroplast DNA of Scots Pine (Pinus sylvestris L.) in Asia and Eastern Europe. Russ J Genet 50(6):577–585. doi:10.1134/S1022795414040127

    Article  CAS  Google Scholar 

  • Soto A, Robledo-Arnuncio JJ, Gonzalez-Martinez SC, et al. (2010) Climatic niche and neutral genetic diversity of the six Iberian pine species: a retrospective and prospective view. Mol Ecol 19:1396–1409. doi:10.1111/j.1365-294X.2010.04571.x

    Article  CAS  PubMed  Google Scholar 

  • Spellman GM, Klicka J (2006) Testing hypotheses of Pleistocene population history using coalescent simulations: phylogeography of the pygmy nuthatch (Sitta pygmaea). Proc R Soc B 273:3057–3063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stampfli G, Borel G, Cavazza W, et al (2002) The paleotectonic atlas of the periTethyan domain: European Geophysical Society, CD-ROM

  • Stefanov B (1941/1942) Geographical distribution of coniferous species and their form in nature. Godichnik na Sofiiskia Darjaven Universitet, Sofia, (Bulgaria), XIX and XX, 1–88 [in Bulgarian]

  • Stefanov B (1943) The phyto-geographical elements of Bulgaria. Thesis of Bulgarian Academy of Sciences, Faculty of Nature and Mathematics, Sofia, (Bulgaria), vol. XXXIX, 19:1–121 [in Bulgarian]

  • Stewart JR (2003) Comment on ‘Buffered tree population changes in a Quaternary refugium: evolutionary implications’. Science 299:825a. doi:10.1126/science.1079388

  • Stewart JR, Dalen L (2008) Is the glacial refugium concept relevant for northern species? A comment on Pruett and Winker 2005. Clim Chang 86:1–2. doi:10.1007/s10584-007-9366-9

    Article  Google Scholar 

  • Stewart JR, Lister AM, Barnes I et al (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc B (277): 661–671; DOI:10.1098/rspb.2009.1272.

  • Svenning JC, Skov F (2004) Limited filling of the potential range in European tree species. Ecol Lett 1:565–573

    Article  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy AG, et al. (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  CAS  PubMed  Google Scholar 

  • Terrab A, Paun O, Talavera S, et al. (2006) Genetic diversity and population structure in natural populations of Moroccan Atlas cedar (Cedrus atlantica; Pinaceae) determined with cpSSR markers. Am J Bot 93:1274–1280. doi:10.3732/ajb.93.9.1274

    Article  CAS  PubMed  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 

  • Vinceti B, Loo J, Gaisberger H, et al. (2013) Conservation priorities for Prunus africana defined with the aid of spatial analysis of genetic data and climatic variables. PLoS One 8(3):e59987. doi:10.1371/journal.pone.0059987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walter R, Epperson BK (2005) Geographic pattern of genetic diversity in Pinus resinosa: contact zone between descendants of glacial refugia. Am J Bot 92(1):92–100

    Article  PubMed  Google Scholar 

  • Wang B, Mahani MK, Ng WL, et al. (2014) Extremely low nucleotide polymorphism in Pinus krempfii Lecomte, a unique flat needle pine endemic to Vietnam. Ecol Evol 4(11):2228–2238. doi:10.1002/ece3.1091

    PubMed  PubMed Central  Google Scholar 

  • Wang Y, Jiang H, Peng S, et al. (2011) Genetic structure in fragmented populations of Hippophae rhamnoides ssp. sinensis in China investigated by ISSR and cpSSR markers. Plant Syst Evol 295(1/4):97–107 http://www.jstor.org/stable/43558222

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wilson IJ, Weale ME, Balding DJ (2003) Inferences from DNA data: population histories, evolutionary processes and forensic match probabilities. J R Stat Soc A 166:155–201

    Article  Google Scholar 

  • Wright S (1979) Evolution and the genetics of populations, vol. 4. Variability within and among natural populations. Chicago, 580 pp

Download references

Acknowledgments

We would like to thank Irena M. Naydenova and T&T for their technical assistance; the two anonymous organisations for their financial support; and 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 and supplied 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) and Miss Honor Hedges (CFB-Kingston, ON, Canada) for the careful English revision of this manuscript.

Author information

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

    Alexander Alexandrov, Veselka Gyuleva & Georgi Hinkov

  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, 11000, Belgrade, Serbia

    Biljana Nikolic

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

    Venceslas Goudiaby

  8. Faculty of forestry, University of Sarajevo, 20 Zagrebacka, Sarajevo, Bosnia and Herzegovina

    Faruk Bogunic

  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. UMR5023 CNRS-Université Lyon 1, 43 Bd 11 novembre 1918, F-69622, Villeurbanne Cedex, France

    Christopher Carcaillet

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

    Adrian Escudero Alcantara

  14. Science Faculty, Department of Biology, Ecology Program, Anadolu University, Biyoloji Bolumu, 26470, Eskisehir, Turkey

    Cengiz Ture

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

    Suleyman Gulcu

  16. Dipartimento di Biologia, Università di Pisa, I-56126, Pisa, Italy

    Lorenzo Peruzzi

  17. Faculté des Sciences, Université Mohamed Premier, Oujda, 63, rue Al maqdis Alqods, 60000, Oujda, Maroc

    Salim Kamary

  18. Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bul. Despota Stefana 142, 11000, Belgrade, Serbia

    Srdjan Bojovic

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

    Anatoly Tsarev

Authors
  1. Krassimir D. Naydenov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michel K. Naydenov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander Alexandrov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kole Vasilevski
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Veselka Gyuleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vlado Matevski
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Biljana Nikolic
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Venceslas Goudiaby
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Faruk Bogunic
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Despina Paitaridou
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Andreas Christou
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Irina Goia
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Christopher Carcaillet
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Adrian Escudero Alcantara
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Cengiz Ture
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Suleyman Gulcu
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Lorenzo Peruzzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Salim Kamary
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Srdjan Bojovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Georgi Hinkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Anatoly Tsarev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Krassimir D. Naydenov.

Additional information

Communicated by Z. Kaya

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

Electronic supplementary material

ESM 1

(DOC 2578 kb)

ESM 2

(XLS 156 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Naydenov, K.D., Naydenov, M.K., Alexandrov, A. et al. Ancient split of major genetic lineages of European Black Pine: evidence from chloroplast DNA . Tree Genetics & Genomes 12, 68 (2016). https://doi.org/10.1007/s11295-016-1022-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-016-1022-y

Keywords

Search

Navigation