Log in

Genetic variation of Central European oaks: shaped by evolutionary factors and human intervention?

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

Abstract

Oak species (Quercus spp.) in Central Europe grow on a relatively wide range of sites. Due to the economic importance of oak for its wood and other products, oak forests have long been managed by humans. This raises the question whether adaptation and/or human activities—especially the moving of propagules—have left their footprints on the genetic variation of oak populations. To address this question, we focused on the Upper Rhine Valley, a densely populated area today that was settled by humans early on. Here, the three most common native Central European oak species can be found. We studied their genetic variation across a large number of oak stands, growing on different sites and having different silvicultural histories, using neutral and EST-derived microsatellite markers. At the interspecific level, we showed that Quercus robur is relatively well delimited, while Quercus petraea and Quercus pubescens are more closely related. Natural hybridization might explain the increased genetic introgression between these two species. Within species, we found a low differentiation among populations of Q. robur and Q. petraea. In spite of forest fragmentation, we detected no spatial genetic barriers. However, we found that populations of Q. pubescens, a species with a marginal distribution in the study area were spatially structured. Genetic drift but also unidirectional introgressive hybridization with Q. petraea may account for this. Regarding the question of adaptation, we considered soil flooding, texture, drainage, and calcium carbonate in the upper horizons as physiologically important site condition variables. But with multivariate statistics, we could not find any significant effects of these parameters on genetic differentiation. Although there was no evidence for natural selection due to adaptation in stands of Q. robur, we demonstrated that age had a significant effect on their genetic variation and that stands established after the end of the Second World War had higher genetic diversity. We interpret these findings as being the result of an increase in large-scale transfers of reproductive materials during this time period and discuss arguments supporting this hypothesis. Finally, we consider the implications of these results for forest management.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Brazil)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aas G (1989) Untersuchungen zur Trennung und Kreuzbarkeit von Stiel-und Traubeneiche (Quercus robur L. und Quercus petraea (Matt.) Liebl.). Doctoral Dissertation, Technische Universität München, Munich

  • Abadie P, Roussel G, Dencausse B, Bonnet C, Bertocchi E, Louvet J-M, Kremer A, Garnier-Géré P (2012) Strength, diversity and plasticity of postmating reproductive barriers between two hybridizing oak species (Quercus robur L. and Quercus petraea (Matt) Liebl.). J Evol Biol 25:157–173

    Article  CAS  PubMed  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Behre K-E (1988) The role of man in European vegetation history. In: Huntley B, Webb T III (eds) Vegetation history. Springer, Netherlands, pp 633–672

    Chapter  Google Scholar 

  • Bingham J, Sudarsanam S (2000) Visualizing large hierarchical clusters in hyperbolic space. Bioinformatics 16:660–661

    Article  CAS  PubMed  Google Scholar 

  • BLE (2013a) Forstliche Herkunftsgebiete (HKG) der Baumarten, die unter das FoVG fallen: Quercus robur L. Stieleiche. Available from: <http://fgrdeu.genres.de/index.php?tpl=fv_hkg&id_art=49> (accessed 3.11.14)

  • BLE (2013b) Forstliche Herkunftsgebiete (HKG) der Baumarten, die unter das FoVG fallen: Quercus petraea (Matt.) Liebl. Traubeneiche. Available from: <http://fgrdeu.genres.de/index.php?tpl=fv_hkg&id_art=47> (accessed 3.11.14)

  • Boeuf R (2014) Les végétations forestières d’ Alsace, vol 1. Imprimerie Scheuer, Drulingen

    Google Scholar 

  • Brewer S, Cheddadi R, de Beaulieu JL, Reille M (2002) The spread of deciduous Quercus throughout Europe since the last glacial period. Forest Ecol Manag 156:27–48

    Article  Google Scholar 

  • Bruschi P, Vendramin GG, Bussotti F, Grossoni P (2000) Morphological and molecular differentiation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. (Fagaceae) in Northern and Central Italy. Ann Bot 85:325–333

    Article  Google Scholar 

  • Buschbom J, Yanbaev Y, Degen B (2011) Efficient long-distance gene flow into an isolated relict oak stand. J Hered 102:464–472

    Article  PubMed  Google Scholar 

  • Chybicki IJ, Oleksa A, Kowalkowska K, Burczyk J (2012) Genetic evidence of reproductive isolation in a remote enclave of Quercus pubescens in the presence of cross-fertile species. Plant Syst Evol 298:1045–1056

    Article  Google Scholar 

  • Curtu AL, Gailing O, Finkeldey R (2009) Patterns of contemporary hybridization inferred from paternity analysis in a four-oak-species forest. BMC Evol Biol 9:284

    Article  PubMed Central  PubMed  Google Scholar 

  • Derory J, Scotti-Saintagne C, Bertocchi E, Le Dantec L, Graignic N, Jauffres A, Casasoli M, Chancerel E, Bodenes C, Alberto F, Kremer A (2010) Contrasting relations between diversity of candidate genes and variation of bud burst in natural and segregating populations of European oaks. Heredity 105:401–411

    Article  CAS  PubMed  Google Scholar 

  • Diniz-Filho JAF, Soares TN, Lima JS, Dobrovolski R, Landeiro VL, de Campos Telles MP, Rangel TF, Bini LM (2013) Mantel test in population genetics. Genet Mol Biol 36:475–485

    Article  PubMed Central  PubMed  Google Scholar 

  • Dow B, Ashley M, Howe H (1995) Characterization of highly variable (GA/CT) n microsatellites in the bur oak, Quercus macrocarpa. Theor Appl Genet 91:137–141

    Article  CAS  PubMed  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    Article  CAS  PubMed  Google Scholar 

  • Dupouey JL, Badeau V (1993) Morphological variability of oaks (Quercus robur L, Quercus petraea (Matt) Liebl, Quercus pubescens Willd) in northeastern France: preliminary results. Ann Sci For 50(Suppl1):35–40

    Article  Google Scholar 

  • Durand J, Bodénès C, Chancerel E et al (2010) A fast and cost-effective approach to develop and map EST-SSR markers: oak as a case study. BMC Genomics 11:570

    Article  PubMed Central  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Felsenstein J (2002) PHYLIP: phylogeny inference package. Version 3(6):a3

    Google Scholar 

  • Gailing O, Wachter H, Schmitt H, Curtu A, Finkeldey R (2007) Characterization of different provenances of Slavonian pedunculate oaks (Quercus robur L.) in Munsterland (Germany) with chloroplast DNA markers: PCR-RFLPs and chloroplast microsatellites. Allg Forst Jagdztg 178:85–90

    Google Scholar 

  • Gerber S, Chadœuf J, Gugerli F, Lascoux M, Buiteveld J, Cottrell J, Dounavi A, Fineschi S, Forrest LL, Fogelqvist J, Goicoechea P, Jensen JS, Salvini D, Vendramin GG, Kremer A (2014) High rates of gene flow by pollen and seed in oak populations across Europe. PLoS ONE 9, e85130

    Article  PubMed Central  PubMed  Google Scholar 

  • Goepp S (2007) Origine, histoire et dynamique des Hautes-Chaumes du massif vosgien. Déterminismes environnementaux et actions de l’Homme. Doctoral Dissertation. Université Luis-Pasteur, Strasbourg

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Grivet D, Sork VL, Westfall RD, Davis FW (2008) Conserving the evolutionary potential of California valley oak (Quercus lobata Née): a multivariate genetic approach to conservation planning. Mol Ecol 17:139–156

    Article  PubMed  Google Scholar 

  • Herzog S (1996) Genetic inventory of European oak populations: consequences for breeding and gene conservation. Ann Sci For 53:783–793

    Article  Google Scholar 

  • Herzog S, Krabel D (1999) Genetic structures of a flooded and a non-flooded oak (Quercus robur) population from the floodplains of the Rhein river. Ekológia (Bratislava) 18:160–163

    Google Scholar 

  • Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, Frascaria-Lacoste N, Hardy OJ, Vekemans X, Vendramin GG (2004) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Mol Ecol 13:3437–3452

    Article  CAS  PubMed  Google Scholar 

  • Homolka A, Schueler S, Burg K, Fluch S, Kremer A (2013) Insights into drought adaptation of two European oak species revealed by nucleotide diversity of candidate genes. Tree Genet Genom 9:1179–1192

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed Central  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Kampfer S, Lexer C, Glössl J, Steinkellner H (1998) Characterization of (GA) n microsatellite loci from Quercus robur. Hereditas 129:183–186

    Article  CAS  Google Scholar 

  • König AO, Ziegenhagen B, van Dam BC, Csaikl UM, Coart E, Degen B, Burg K, de Vries SMG, Petit RJ (2002) Chloroplast DNA variation of oaks in western Central Europe and genetic consequences of human influences. For Ecol Manag 156:147–166

    Article  Google Scholar 

  • Krabel D, Liesebach M, Schneck V, Wolf H (2010) Transfer von saat-und pflanzgut innerhalb Europas. Forst und Holz 65:2–7

    Google Scholar 

  • Kremer A, Petit RJ, Zanetto A, Fougère V, Ducousso A, Wagner D, Chauvin C (1991) Nuclear and organelle gene diversity in Quercus robur and Q. petraea. In: Müller-Starck G and Ziehe M (eds) Genetic variation in European populations of forest trees. Sauerländer’s Verlag, Frankfurt am Main, pp. 125–140

  • Küster H (1996) Auswirkungen von klimaschwankungen und menschlicher landschaftsnutzung auf die arealverschiebung von pflanzen und die ausbildung mitteleuropäischer wälder. Forstwiss Cent Ver Mit Tharandter Forstl Jahrb 115:301–320

    Article  Google Scholar 

  • Lepais O, Gerber S (2011) Reproductive patterns shape introgression dynamics and species succession within the European white oak species complex. Evolution 65:156–170

    Article  PubMed  Google Scholar 

  • Lepais O, Petit RJ, Guichoux E, Lavabre JE, Alberto F, Kremer A, Gerber S (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242

    Article  CAS  PubMed  Google Scholar 

  • Lepais O, Roussel G, Hubert F, Kremer A, Gerber S (2013) Strength and variability of postmating reproductive isolating barriers between four European white oak species. Tree Genet Genomes 9:841–853

    Article  Google Scholar 

  • MAAF (2014) Liste de régions de provenance des espèces forestières - Liste actualisée en mai 2014. Available from: <http://agriculture.gouv.fr/Fournisseurs-especes-et-provenances-forestieres> (accessed 3.11.14)

  • Müller B (1999) Variation und Hybridisierung von Quercus pubescens. Eidgenössische Technische Hochschule Zürich

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Neophytou C (2014) Bayesian clustering analyses for genetic assignment and study of hybridization in oaks: effects of asymmetric phylogenies and asymmetric sampling schemes. Tree Genet Genomes 10:273–285

    Article  Google Scholar 

  • Neophytou C, Michiels HG (2013) Upper Rhine Valley: a migration crossroads of middle European oaks. Forest Ecol Manage 304:89–98

    Article  Google Scholar 

  • Oberdorfer E (1992) Süddeutsche Pflanzengesellschaften Band IV (Wälder und Gebüsche) Fischer Verlag, Stuttgart

  • Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry H, Stevens H, Wagner H (2013) VEGAN: community ecology package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan

  • Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Petit RJ, Csaikl UM, Bordács S, Burg K, Coart E, Cottrell J, van Dam B, Deans JD, Dumolin-Lapègue S, Fineschi S (2002) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manag 156:5–26

    Article  Google Scholar 

  • Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164

    Article  CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pritchard JK, Pickrell JK, Coop G (2010) The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol 20:R208–R215

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, <http://www.R-project.org/>

  • Reif A, Gärtner S (2007) Die natürliche Verjüngung der laubabwerfenden Eichenarten Stieleiche (Quercus robur L.) und Traubeneiche (Quercus petraea Liebl.)–eine Literaturstudie mit besonderer Berücksichtigung der Waldweide. Waldökologie online 5:79–116

    Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Sebald O, Seybold S, Philippi G, Wörz A, Kleinsteuber A, Gottschlich G, Böhling N, Baumann H (1998) Die Farn-und Blütenpflanzen Baden-Württembergs. Ulmer, Stuttgart

  • Sork VL, Davis FW, Westfall R, Flint A, Ikegami M, Wang H, Grivet D (2010) Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Née) in the face of climate change. Mol Ecol 19:3806–3823

    Article  PubMed  Google Scholar 

  • Steinkellner H, Lexer C, Turetschek E, Glössl J (1997) Conservation of (GA)n microsatellite loci between Quercus species. Mol Ecol 6:1189–1194

    Article  CAS  Google Scholar 

  • Streiff R, Ducousso A, Lexer C, Steinkellner H, Gloessl J, Kremer A (1999) Pollen dispersal inferred from paternity analysis in a mixed oak stand of Quercus robur L. and Q. petraea (Matt.) Liebl. Mol Ecol 8:831–841

    Article  Google Scholar 

  • Uhl A, Reif A, Gärtner S (2008) Naturverjüngung der Stieleiche (Quercus robur L.) im Gebiet der „Trockenaue “am südlichen Oberrhein (Südwestdeutschland). Carolinea 66:15–34

    Google Scholar 

  • Vähä J-P, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72

    Article  PubMed  Google Scholar 

  • Vidalis A, Curtu AL, Finkeldey R (2013) Novel SNP development and analysis at a NADP+-specific IDH enzyme gene in a four species mixed oak forest. Plant Biol 15:126–137

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Zenni RD, Lamy J-B, Lamarque LJ, Porté AJ (2014) Adaptive evolution and phenotypic plasticity during naturalization and spread of invasive species: implications for tree invasion biology. Biol Invasions 16:635–644

    Article  Google Scholar 

Download references

Acknowledgments

The current study has been conducted within the framework of the Interreg-IV project “The regeneration of the oaks in the Upper Rhine lowlands,” funded by the European Regional Development Fund (ERDF), the regional government authority of Baden-Württemberg in Freiburg (Regierungspräsidium Freiburg; RPF), the National Office of Forests (Office National des Forêts; ONF) in France, and the Regional Directory of Food, Agriculture and Forestry of Alsace (Direction Régionale de l’Alimentation, de l’Agriculture et de la Forêt d’Alsace; DRAAF). We express our gratitude to all of the people from the ONF, RPF, and the FVA who worked for the project in the field, in the lab, or in the office. We thank three anonymous reviewers for providing valuable comments on this article. We thank Bernhard Thiel for improving the English of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Data archiving statement

Genotypic data used for this study are available at Dryad: 10.5061/dryad.b64b4.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charalambos Neophytou.

Additional information

Communicated by A. Kremer

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 20 kb)

ESM 2

(XLSX 179 kb)

ESM 3

(PDF 86 kb)

ESM 4

(XLSX 45 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Neophytou, C., Gärtner, S.M., Vargas-Gaete, R. et al. Genetic variation of Central European oaks: shaped by evolutionary factors and human intervention?. Tree Genetics & Genomes 11, 79 (2015). https://doi.org/10.1007/s11295-015-0905-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-015-0905-7

Keywords

Navigation