Skip to main content
Log in

Interfertile oaks in an island environment: I. High nuclear genetic differentiation and high degree of chloroplast DNA sharing between Q. alnifolia and Q. coccifera in Cyprus. A multipopulation study

  • Original Paper
  • Published:
European Journal of Forest Research Aims and scope Submit manuscript

Abstract

The evergreen Quercus alnifolia and Q. coccifera form the only interfertile pair of oak species growing in Cyprus. Hybridization between the two species has already been observed and studied morphologically. However, little evidence exists about the extent of genetic introgression. In the present study, we aimed to study the effects of introgressive hybridization mutually on both chloroplast and nuclear genomes. We sampled both pure and mixed populations of Q. alnifolia and Q. coccifera from several locations across their distribution area in Cyprus. We analyzed the genetic variation within and between species by conducting analysis of molecular variance (AMOVA) based on nuclear microsatellites. Population genetic structure and levels of admixture were studied by means of a Bayesian analysis (STRUCTURE simulation analysis). Chloroplast DNA microsatellites were used for a spatial analysis of genetic barriers. The main part of the nuclear genetic variation was explained by partition into species groups. High interspecific differentiation and low admixture of nuclear genomes, both in pure and mixed populations, support limited genetic introgression between Q. alnifolia and Q. coccifera in Cyprus. On the contrary, chloroplast DNA haplotypes were shared between the species and were locally structured suggesting cytoplasmic introgression. Occasional hybridization events followed by backcrossings with both parental species might lead to this pattern of genetic differentiation.

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

Access this article

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Barbero M, Quezel P (1979) Contribution à l’étude des groupements forestiers de Chypre. Documents Phytosociologiques IV:9–34

    Google Scholar 

  • Belahbib N, Pemonge M, 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 10:2003–2012

    Article  PubMed  CAS  Google Scholar 

  • Boavida LC, Silva JP, Feijó JA (2001) Sexual reproduction in the cork oak (Quercus suber L). II. Crossing intra- and interspecific barriers. Sex Plant Reprod 14:143–152

    Article  Google Scholar 

  • 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 102:442–452

    Article  PubMed  CAS  Google Scholar 

  • Butzer KW, Harris SE (2007) Geoarchaeological approaches to the environmental history of Cyprus: explication and critical evaluation. J Archaeol Sci 34:1932–1952

    Article  Google Scholar 

  • Christou A (2001) Cyprus (country report). Mediterranean Oaks Network: Report of the first meeting: 12–14 October 2000-Antalya, Turkey 3

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Craft KJ, Ashley MV (2006) Population differentiation among three species of white oak in northeastern Illinois. Can J Forest Res 36:206–215

    Article  Google Scholar 

  • Curtu AL, Gailing O, Leinemann L, Finkeldey R (2007a) Genetic variation and differentiation within a natural community of five oak species (Quercus spp.). Plant Biol 9:116–126

    Article  PubMed  CAS  Google Scholar 

  • Curtu AL, Gailing O, Finkeldey R (2007b) Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evol Biol 7:218–233

    Article  PubMed  Google Scholar 

  • Darwin C (1859) On the origin of species by natural selection. Murray, London

    Google Scholar 

  • Deguilloux M, Dumolin-Lapègue S, Gielly L, Grivet D, Petit RJ (2003) A set of primers for the amplification of chloroplast microsatellites in Quercus. Mol Ecol Notes 3:24–27

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  CAS  Google Scholar 

  • Fineschi S, Cozzolino S, Migliaccio M, Musacchio A, Innocenti M, Vendramin GG (2005) Sicily represents the Italian reservoir of chloroplast DNA diversity of Quercus ilex L. (Fagaceae). Ann For Sci 62:79–84

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Gugerli F, Walser J, Dounavi K, Holderegger R, Finkeldey R (2007) Coincidence of small-scale spatial discontinuities in leaf morphology and nuclear microsatellite variation of Quercus petraea and Q. robur in a mixed forest. Ann Bot 99:713–722

    Article  PubMed  CAS  Google Scholar 

  • Gugerli F, Brodbeck S, Holderegger R (2008) Utility of multilocus genotypes for taxon assignment in stands of closely related European white oaks from Switzerland. Ann Bot 102:855–863

    Article  PubMed  Google Scholar 

  • Hand R (2006) Supplementary notes to the flora of Cyprus V. Willdenowia 36:761–809

    Google Scholar 

  • Jiménez P, López de Heredia U, Collada C, Lorenzo Z, Gil L (2004) High variability of chloroplast DNA in three Mediterranean evergreen oaks indicates complex evolutionary history. Heredity 93:510–515

    Article  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 

  • Knopf H (2006) Quercus alnifolia Poech. In: Schütt P, Schuck HJ, Lang UM, Roloff A (eds). Enzyklopädie der Holzgewächse 3. Landsberg am Lech, pp 1–7

  • Kremer A, Kleinschmit J, Cottrell J et al (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 156:75–87

    Article  Google Scholar 

  • Lexer C, Kremer A, Petit RJ (2006) Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Mol Ecol 15:2007–2012

    Article  PubMed  CAS  Google Scholar 

  • 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 32:939–949

    Article  Google Scholar 

  • López de Heredia U, Carrión JS, Jiménez P, Collada C, Gil L (2007a) Molecular and palaeoecological evidence for multiple glacial refugia for evergreen oaks on the Iberian Peninsula. J Biogeogr 34:1505–1517

    Article  Google Scholar 

  • López de Heredia U, 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 56:1209–1220

    Article  Google Scholar 

  • Lorenzo Z, Burgarella C, de Heredia UL, Lumaret R, Petit RJ, Soto A, Gil L (2009) Relevance of genetics for conservation policies: the case of Minorcan cork oaks. Ann Bot 104:1069–1076

    Article  PubMed  Google Scholar 

  • 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 104:725–736

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Magri D, Fineschi S, Bellarosa R, Buonamici A, Sebastiani F, Schirone B, Simeone MC, Vnedramin GG (2007) The distribution of Quercus suber chloroplast haplotypes matches the palaeogeographical history of the western Mediterranean. Mol Ecol 16:5259–5266

    Article  PubMed  CAS  Google Scholar 

  • Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation. Hum Biol 76:173–190

    Article  PubMed  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061

    PubMed  CAS  Google Scholar 

  • Minch E, Ruiz-Linares A, Goldstein D, Feldman M, Cavalli-Sforza LL (1995) MICROSAT, The microsatellite distance program. http://human.stanford.edu/ Stanford California: Stanford University

  • Mir C, Jarne P, Sarda V, Bonin A, Lumaret R (2009) Contrasting nuclear and cytoplasmic exchanges between phylogenetically distant oak species (Quercus suber L. and Q. ilex L.) in Southern France: inferring crosses and dynamics. Plant Biol 11:213–226

    Article  PubMed  CAS  Google Scholar 

  • Monmonier M (1973) Maximum-difference barriers: An alternative numerical regionalization method. Geogr Anal 3:245–261

    Google Scholar 

  • Muir G, Schlötterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Mol Ecol 14:549–561

    Article  PubMed  CAS  Google Scholar 

  • Muir G, Fleming CC, Schlotterer C (2000) Species status of hybridizing oaks. Nature 405:1016

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Neophytou C, Palli G, Dounavi A, Aravanopoulos F (2007) Morphological differentiation and hybridization between Quercus alnifolia Poech and Quercus coccifera L. (Fagaceae) in Cyprus. Silvae Genet 56:271–277

    Google Scholar 

  • Neophytou C, Dounavi A, Aravanopoulos F (2008) Conservation of nuclear SSR loci reveals high affinity of Quercus infectoria ssp. veneris A. Kern (Fagaceae) to section Robur. Plant Mol Biol Rep 26:133–141

    Article  CAS  Google Scholar 

  • Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Peakall R, 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 et al (2002) Chloroplast DNA variation in European white oaks: Phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manage 156:5–26

    Article  Google Scholar 

  • Petit RJ, Bodenes 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 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    Article  PubMed  CAS  Google Scholar 

  • Pons O, Petit RJ (1995) Estimation, variance and optimal sampling of gene diversity. Theor Appl Genet 90:462–470

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rubio de Casas R, Cano E, Balaguer L, Perez-Corona E, Manrique E, García-Verdugo C, Vargas P (2007) Taxonomic identity of Quercus coccifera L. in the Iberian Peninsula is maintained in spite of widespread hybridisation, as revealed by morphological, ISSR and ITS sequence data. Flora 202:488–499

    Google Scholar 

  • Salvini D, Bruschi P, Fineschi S, Grossoni P, Kjær ED, Vendramin GG (2009) Natural hybridisation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. within an Italian stand as revealed by microsatellite fingerprinting. Plant Biol 11:758–765

    Article  PubMed  CAS  Google Scholar 

  • Scotti-Saintagne C, Bodénès C, Barreneche T, Bertocchi E, Plomion C, Kremer A (2004) Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. and Q. petraea (Matt.) Liebl.]. Genetics 168:1615–1626

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Soto A, Lorenzo Z, 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 99:601–607

    Article  PubMed  CAS  Google Scholar 

  • Steinkellner H, Fluch S, Turetschek E, Lexer C, Streiff R, Kremer A, Burg K, Glössl J (1997) Identification and characterization of (GA/CT)n- microsatellite loci from Quercus petraea. Plant Mol Biol 33:1093–1096

    Article  PubMed  CAS  Google Scholar 

  • Toumi L, Lumaret R (2001) Allozyme characterisation of four Mediterranean evergreen oak species. Biochem Syst Ecol 29:799–817

    Article  PubMed  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256

    Article  Google Scholar 

  • Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Andreas Christou, Constantinos Kounnamas, Salih Gücel, Zacharias Triftarides, Savvas Protopapas, Petros Anastasiou and the Department of Forests, Republic of Cyprus personnel, for their assistance during plant collections. We are grateful to Dr. Unai López de Heredia for stimulating discussions. This research was conducted in partial fulfillment for the doctorate degree of the first author at Albert-Ludwigs University of Freiburg. During that time, the first author was supported by doctorate scholarships from DAAD and the State of Baden-Württemberg. Partial financial assistance to Filippos Aravanopoulos in the form of two cooperative grants of the Ministry of Natural Resources of Cyprus and the Aristotle University of Thessaloniki is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charalambos Neophytou.

Additional information

Communicated by K. Puettmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TXT 1 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Neophytou, C., Dounavi, A., Fink, S. et al. Interfertile oaks in an island environment: I. High nuclear genetic differentiation and high degree of chloroplast DNA sharing between Q. alnifolia and Q. coccifera in Cyprus. A multipopulation study. Eur J Forest Res 130, 543–555 (2011). https://doi.org/10.1007/s10342-010-0442-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10342-010-0442-8

Keywords

Navigation