Evolutionary Ecology

, Volume 28, Issue 1, pp 55–68 | Cite as

Geographical variation in growth form traits in Quercus suber and its relation to population evolutionary history

Original Paper


Differential selection pressures caused by environmental disparities lead to populations to become differentiated as they adapt to local environments. In addition, natural selection during the species past can contribute to the observed differentiation. In this study, we examine the geographic variation in a set of four traits related to growth and plant architecture in cork oak (Quercus suber) and investigate to what extent this variation is the result of the effects of ongoing evolution in current environments and the past evolutionary history of the species. Cork oak saplings at the common garden trial exhibited differences in plant architecture associated to cpDNA lineage. Eastern lineages, exhibited the lowest apical dominance and highest branchiness, consistent with the analyses in other cork oak trials. In contrast, patterns linked to the evolutionary past were less evident in height and diameter. These results suggest that selective pressures after cpDNA divergence can have blurred patterns in some traits closely related to fitness, while conserving the past evolutionary imprints in plant architectural traits. Introgressed populations did not show significant differentiation in architecture, which suggests that allele exchanges via hybridization have had a limited effect on population differentiation in cork oak. Finally, populations within lineages also showed differences in growth and architecture. Correlation between population architecture and temperature patterns were observed indicating that environmental factors such as climate also could result crucial in the evolution of plant architecture of cork oak within lineages.


Plant architecture Growth adaptation Population ecology Evolutionary history 



We are grateful to Pedro Fernández, Laura Castro, Regina Chambel, José María Climent, Pilar Jiménez, and everyone from the Forestry School of Madrid who collaborated in the setting up of the cork oak common gardens under the EU-concerted action on cork oak, FAIR I CT 95 0202. We would like to thank Salustiano Iglesias and the DGB for the maintenance of the assays. We also thank Santiago de Blas, José Antonio Mancha, Diana Barba, Fernando del Caño and other field assistants for their help during the experiment. This work was funded by the Spanish Ministry of Science (PLASTOFOR, AGL-00536/FOR and and AGL2011-25365/FOR projects). This study was also supported by a González-Esparcia postdoctoral scholarship to JARV.

Supplementary material

10682_2013_9660_MOESM1_ESM.doc (2.8 mb)
Supplementary material 1 (DOC 2896 kb)


  1. Alía R, Gil L, Pardos JA (1995) Performance of 43 Pinus pinaster provenances on 5 locations in Central Spain. Silvae Genet 44:75–81Google Scholar
  2. Aranda I, Castro L, Alía R, Pardos JA, Gil L (2005) Low temperature during winter elicits differential responses among populations of the Mediterranean evergreen cork oak (Quercus suber). Tree Physiol 25:1085–1090PubMedCrossRefGoogle Scholar
  3. Aronson J, Pereira JS, Pausas JC (2009) Cork oak woodlands on edge: ecology, adaptive management and restoration. Island Press, Washington, DCGoogle Scholar
  4. Barthélémy D, Caraglio Y (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann Bot 99:375–407PubMedCrossRefGoogle Scholar
  5. Belahbib N, Pemonge MH, Ouassou A, Sbay H, Kremer A, Petit RJ (2001) Frequent cytoplasmic exchanges between oak species that are not closely related: Quercus suber and Q. ilex in Morocco. Mol Ecol 10:2003–2012PubMedCrossRefGoogle Scholar
  6. Bergin DO, Kimberley MO, Low CB (2008) Provenance variation in Podocarpus totara (D. Don): growth, tree form and wood density on a coastal site in the north of the natural range, New Zealand. For Ecol Manage 255:1367–1378Google Scholar
  7. Bruschi P, Vendramin GG, Bussotti F, Grossoni P (2003) Morphological and molecular diversity among Italian populations of Quercus petraea (Fagaceae). Ann Bot 91:707–716PubMedCrossRefGoogle Scholar
  8. Burgarella C, Lorenzo Z, Jabbour-Zahab R, Lumaret R, Guichoux E, Petit RJ, Soto A, Gil L (2009) Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity 102:442–452PubMedCrossRefGoogle Scholar
  9. Cavender-Bares J, Pahlich A (2009) Molecular, morphological and ecological niche differentiation of sympatric sister oak species, Quercus virginiana and Q. geminata (Fagaceae). Am J Bot 96:1690–1702PubMedCrossRefGoogle Scholar
  10. Comstock JP (2000) Variation in hydraulic architecture and gas- exchange in two desert sub-shrubs, Hymenoclea salsola (T. & G.) and Ambrosia dumosa (Payne). Oecologia 125:1–10CrossRefGoogle Scholar
  11. Cundall EP, Cahalan CM, Connolly T (2003) Early results of ash (Fraxinus excelsior L.) provenance trials at sites in England and Wales. Forestry 76:385–399CrossRefGoogle Scholar
  12. Denk T, Grimm GW, Hemleben V (2005) Patterns of molecular and morphological differentiation in Fagus (Fagaceae): phylogenetic implications. Am J Bot 92:1006–1016PubMedCrossRefGoogle Scholar
  13. Donovan LA, Dudley SA, Rosenthal DM, Ludwig F (2007) Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers. Oecologia 152:13–25PubMedCrossRefGoogle Scholar
  14. Foster SA, McKinnon GE, Steane DA, Potts BM, Vaillancourt RE (2007) Parallel evolution of dwarf ecotypes in the forest tree Eucalyptus globulus. New Phytol 175:370–380PubMedCrossRefGoogle Scholar
  15. Gandour M, Khouja ML, Toumi L, Triki S (2007) Morphological evaluation of cork oak (Quercus suber L.): Mediterranean provenance variability in Tunisia. Ann For Sci 64:549–555CrossRefGoogle Scholar
  16. Gonzalez-Martinez SC, Alia R, Gil L (2002) Population genetic structure in a Mediterranean pine (Pinus pinaster Ait.): a comparison of allozyme markers and quantitative traits. Heredity 89:199–206PubMedCrossRefGoogle Scholar
  17. Hatziskakis S, Tsiripidis I, Papageorgiou AC (2011) Leaf morphological variation in beech (Fagus sylvatica L.) populations in Greece and its relation to their post-glacial origin. Bot J Linn Soc 165:422–436CrossRefGoogle Scholar
  18. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276Google Scholar
  19. Housman DC, Price MV, Redak RA (2002) Architecture of coastal and desert Encelia farinosa (Asteraceae): consequences of plastic and heritable variation in leaf characters. Am J Bot 89:1303–1310PubMedCrossRefGoogle Scholar
  20. Jiménez P, López de Heredia U, Collada C, Lorenzo Z, Gil L (2004) High varaiability of chloroplast DNA in three Mediterranean evergreen oaks indicates complex evolutionary history. Heredity 93:510–515PubMedCrossRefGoogle Scholar
  21. Körrner Ch, Cochrane P (1983) Influence of plant physiognomy on leaf temperature on clear midsummer days in the Snowy Mountains, south-eastern Australia. Acta Oecol, Oecol Plant 4:117–124Google Scholar
  22. Kremer A, Kleinschmit J, Cottrell J, Cundall EP, Deans JD, Ducousso A, König AO, Lowe AJ, Munro RC, Petit RJ, Stephan BR (2002) Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks? For Ecol Manage 156:75–85CrossRefGoogle Scholar
  23. Leinonen T, O’Hara RB, Cano JM, Merila J (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J Evol Biol 21:1–17PubMedGoogle Scholar
  24. Linares JC (2011) Biogeography and evolution of Abies (Pinaceae) in the Mediterranean Basin: the roles of long-term climatic change and glacial refugia. J Biogeogr 38:619–630CrossRefGoogle Scholar
  25. López de Heredia U (2006) La diversidad en las especies forestales: un cambio de escala. El ejemplo del alcornoque. Ecosistemas 15:24–33Google Scholar
  26. López de Heredia U, Jiménez P, Díaz-Fernández P, Gil L (2005) The Balearic islands: a reservoir of cpDNA genetic variation for evergreen oaks. J Biogeogr 32:939–949CrossRefGoogle Scholar
  27. López de Heredia U, Carrión JS, Jiménez P, Collada C, Gil L (2007a) Molecular and palaeobotanical evidence for multiple glacial refugia for evergreen oaks on the Iberian Peninsula. J Biogeogr 34:1505–1517Google Scholar
  28. López de Heredia UL, Jiménez P, Collada C, Simeone MC, Bellarosa R, Schirone B, Cervera MT, Gil L (2007b) Multi-marker phylogeny of three evergreen oaks reveals vicariant patterns in the Western Mediterranean. Taxon 56:1209–1220CrossRefGoogle Scholar
  29. Lumaret R, Jabbour-Zahab R (2009) Ancient and current gene flow between two distantly related Mediterranean oak species, Quercus suber and Q. ilex. Ann Bot 104:725–736PubMedCrossRefGoogle Scholar
  30. Lumaret R, Mir C, Michaud H, Raynal V (2002) Phylogeographical variation of chloroplast DNA in holm oak (Quercus ilex L.). Mol Ecol 11:2327–2336PubMedCrossRefGoogle Scholar
  31. Lumaret R, Tryphon-Dionnet M, Michaud H, Sanuy A, Ipotesi E, Born C, Mir C (2005) Phylogeographical variation of chloroplast DNA in cork oak (Quercus suber). Ann Bot 96:853–861PubMedCrossRefGoogle Scholar
  32. Magri D, Fineschi S, Bellarosa R, Buonamici A, Sebastiani F, Schirone B, Simeone MC, Vendramin GG (2007) The distribution of Quercus suber chloroplast haplotypes matches the palaeogeographical history of the western Mediterranean. Mol Ecol 16:5259–5266PubMedCrossRefGoogle Scholar
  33. Mallet J (2007) Hybrid speciation. Nature 446:279–283PubMedCrossRefGoogle Scholar
  34. Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903CrossRefGoogle Scholar
  35. Mir C, Toumi L, Jarne P, Sarda V, Di Giusto F, Lumaret R (2006) Endemic North African Quercus afares Pomel originates from hybridisation between two genetically very distant oak species (Q. suber L. and Q. canariensis Willd.): evidence from nuclear and cytoplasmic markers. Heredity 96:175–184PubMedCrossRefGoogle Scholar
  36. Ortego J, Bonal R (2010) Natural hybridisation between kermes (Quercus coccifera, L.) and holm oaks (Q. ilex, L.) revealed by microsatellite markers. Plant Biol 12:234–238PubMedCrossRefGoogle Scholar
  37. Papageorgiou AC, Vidalis A, Gailing O, Tsiripidis I, Hatziskakis S, Boutsios S, Galatsidas S, Finkeldey R (2008) Genetic variation of beech (Fagus sylvatica L.) in Rodopi (N.E. Greece). Eur J For Res 127:81–88CrossRefGoogle Scholar
  38. Pearcy RW, Valladares F, Wright SJ, Lasso E (2004) A functional analysis of the crown architecture of tropical forest Psychotria species: do species vary in light capture efficiency and consequently in carbon gain and growth? Oecologia 139:163–167PubMedCrossRefGoogle Scholar
  39. Petit RJ, Brewer S, Bordacs S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, van Dam B, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicoechea PG, Jensen JS, Konig AO, Lowe AJ, Madsen SF, Matyas G, Munro RC, Popescu F, Slade D, Tabbener H, Vries SGM, Ziegenhagen B, Beaulieu JL, Kremer A (2002) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manage 156:49–74Google Scholar
  40. Petit RJ, Bodenes C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–154Google Scholar
  41. Petit RJ, Duminil J, Fineschi S et al (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701PubMedCrossRefGoogle Scholar
  42. Ramírez-Valiente JA, Valladares F, Gil L, Aranda I (2009a) Population differences in juvenile survival under increasing drought are mediated by seed size in cork oak (Quercus suber L.). For Ecol Manage 257:1676–1683CrossRefGoogle Scholar
  43. Ramírez-Valiente JA, Lorenzo Z, Soto A, Valladares F, Gil L, Aranda I (2009b) Elucidating the role of genetic drift and natural selection in cork oak differentiation regarding drought tolerance. Mol Ecol 18:3803–3815PubMedCrossRefGoogle Scholar
  44. Ramírez-Valiente JA et al (2010) Phenotypic plasticity and local adaptation in leaf ecophysiological traits of 13 contrasting cork oak populations under different water availabilities. Tree Physiol 30:618–627PubMedCrossRefGoogle Scholar
  45. Ramírez-Valiente JA, Valladares F, Delgado A, Granados S, Aranda I (2011) Factors affecting cork oak growth under dry conditions: local adaptation and contrasting additive genetic variance within populations. Tree Genet Genome 7:285–295CrossRefGoogle Scholar
  46. Rieseberg LH, Wendel J (1993) Introgression and its consequences in plants. In: Harrison R (ed) Hybrid Zones and the Evolutionary Process. Oxford University Press, New YorkGoogle Scholar
  47. Scotti-Saintagne C, Mariette S, Porth I, Goicoechea PG, Barreneche T, Bodenes C, Burg K, Kremer A (2004) Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. and Q. petraea (Matt.) Liebl.]. Genetics 168:1615–1626PubMedCrossRefGoogle Scholar
  48. Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207PubMedCrossRefGoogle Scholar
  49. Soto A, Lorenzo ZR, Gil L (2007) Differences in fine-scale genetic structure and dispersal in Quercus ilex L. and Q. suber L.: consequences for regeneration of Mediterranean open woods. Heredity 99:601–607PubMedCrossRefGoogle Scholar
  50. Svenning JC, Skov F (2005) The relative roles of environment and history as controls of tree species composition and richness in Europe. J Biogeogr 32:1019–1033CrossRefGoogle Scholar
  51. Toumi L, Lumaret R (1998) Allozyme variation in cork oak (Quercus suber L): the role of phylogeography, genetic introgression by other Mediterranean oak species and human activities. Theor Appl Genet 97:647–656CrossRefGoogle Scholar
  52. Valbuena-Carabaña M, González-Martínez SC, Hardy OJ, Gil L (2007) Fine-scale spatial genetic structure in mixed oak stands with different levels of hybridization. Mol Ecol 16:1207–1219PubMedCrossRefGoogle Scholar
  53. Wang Y, Li J (2005) Genes controlling plant architecture. Curr Opin Biotechnol 17:1–7Google Scholar
  54. Wang Y, Li J (2008) Molecular basis of plant architecture. Ann Rev Plant Biol 59:253–279CrossRefGoogle Scholar
  55. White TL, Adams WT, Neale DB (2007) Forest genetics. CAB International, Wallingford, UKCrossRefGoogle Scholar
  56. Willyard A, Cronn R, Liston A (2009) Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Mol Phylogenet Evol 52:498–511PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Forest Ecology and GeneticsINIA, Forest Research CentreMadridSpain

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