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Interfertile oaks in an island environment. II. Limited hybridization between Quercus alnifolia Poech and Q. coccifera L. in a mixed stand

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Abstract

Hybridization and introgression between Quercus alnifolia Poech and Q. coccifera L. is studied by analyzing morphological traits, nuclear and chloroplast DNA markers. The study site is a mixed stand on Troodos Mountains (Cyprus), and the analyzed material includes both adult trees and progenies of specific mother trees. Multivariate analysis of morphological traits shows that the two species can be well distinguished using simple leaf morphometric parameters. A lower genetic diversity in Q. alnifolia than in Q. coccifera and a high interspecific differentiation between the two species are supported by an analysis of nuclear and chloroplast microsatellites. The intermediacy of the four designated hybrids is verified by both leaf morphometric and genetic data. Analysis of progeny arrays provides evidence that interspecific crossings are rare. This finding is further supported by limited introgression of chloroplast genomes. Reproductive barriers (e.g. asynchronous phenology, postzygotic incompatibilities) might account for this result. A directionality of interspecific gene flow is indicated by a genetic assignment analysis of effective pollen clouds with Q. alnifolia acting as pollen donor. Differences in flowering phenology and species distribution in the stand may have influenced the direction of gene flow and the genetic differentiation among effective pollen clouds of different mother trees within species.

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References

  • Aravanopoulos FA (2005) Phenotypic variation and population relationships of chestnut (Castanea sativa) in Greece, revealed by multivariate analysis of leaf morphometrics. Acta Hort 693:230–240

    Google Scholar 

  • Bacilieri R, Ducousso A, Petit RJ, Kremer A (1996) Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution 50:900–908

    Article  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 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171. Université de Montpellier II, Montpellier (France)

    Google Scholar 

  • Benzécri JP, Bellier L (1973) L’analyse des données: Benzécri, J.-P. et al. L’analyse des correspondances. Dunod, Paris

    Google Scholar 

  • Bianco P, Schirone B (1985) On Quercus coccifera L. s.l.: variation in reproductive phenology. Taxon 34:436–439

    Article  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 

  • Chatziphilippidis G (2006) Quercus coccifera Linné, 1753. In: Schütt P, Schuck HJ, Lang UM, Roloff A (eds) Enzyklopädie der Holzgewächse 3. Landsberg am Lech.

  • 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 

  • Dickinson TA, Parker WH, Strauss RE (1987) Another approach to leaf shape comparisons. Taxon, pp 1–20

  • Dodd RS, Afzal-Rafii Z (2004) Selection and dispersal in a multispecies oak hybrid zone. Evolution 58:261–269

    PubMed  Google Scholar 

  • Finkeldey R, Mátyás G (2003) Genetic variation of oaks (Quercus spp.) in Switzerland. 3. Lack of impact of postglacial recolonization history on nuclear gene loci. Theor Appl Genet 106:346–352

    PubMed  CAS  Google Scholar 

  • Fisher RA (1936) Multiple measurements in taxonomic problems. Ann Eugen 7:179–188

    Article  Google Scholar 

  • Gillet EM (1997) Maximum likelihood estimators of the gametic contributions to single-plant progenies. Biometrics 53:504–523

    Article  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 

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

    Google Scholar 

  • Jimenez P, de Heredia UL, 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  CAS  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.

  • Kremer A, Dupouey JL, Deans JD, Cottrell J, Csaikl U, Finkeldey R, Espinel S, Jensen J, Kleinschmit J, Van Dam B (2002) Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Ann For Sci 59:777–787

    Article  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  PubMed  CAS  Google Scholar 

  • López de Heredia U, Jiménez P, Simeone MC, Bellarosa R, Schirone B, Cervera MT, Gil L (2007) Multi-marker phylogeny of three evergreen oaks reveals vicariant patterns in the Western Mediterranean. Taxon 56:1209–1220

    Article  Google Scholar 

  • Meikle RD (1977) Flora of Cyprus 1–2. Bentham-Moxon Trust, Kew

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  • 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 

  • Neophytou C, Dounavi A, Fink S, Aravanopoulos F (2010a) 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 For Res. doi:10.1007/s10342-010-0442-8

  • Neophytou C, Aravanopoulos F, Fink S, Dounavi A (2010b) Detecting interspecific and geographic differentiation patterns in two interfertile oak species (Quercus petraea (Matt.) Liebl. and Q. robur L.) using small sets of microsatellite markers. For Ecol Manag 259(10):2026–2035

    Article  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 ROD, Smouse PE (2005) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A (1997a) Chloroplast DNA footprints of postglacial recolonization by oaks. Proc Natl Acad Sci USA 94:9996–10001

    Article  PubMed  CAS  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1997b) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Google Scholar 

  • Petit RJ, Csaikl UM, Bordács S, Burg K, Coart E, Cottrell J, Dam BV, Deans JD, Dumolin-Lapègue S, Fineschi S, Finkeldey R, Amanda GlazI, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Olalde M, Pemonge M, Popescu F, Slade D, Tabbener H, Taurchini D, Vries SGMD, Ziegenhagen B, Kremer A (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 

  • Pimentel RA (1979) Morphometrics: the multivariate analysis of biological data. Kendall/Hunt Dubuque, Iowa

    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 

  • Rushton BS (1993) Natural hybridization within the genus Quercus L. Ann Sci For 50:18 pp.

    Google Scholar 

  • Salvini D, Bruschi P, Fineschi S, Grossoni P, Kjaer 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 

  • Smouse PE, Dyer RJ, Westfall RD, Sork VL (2001) Two-generation analysis of pollen flow across a landscape. I. Male gamete heterogeneity among females. Evolution 55:260–271

    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 

  • Streiff R, Ducousso A, Lexer C, Steinkellner H, Glössl 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 

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

    Article  CAS  Google Scholar 

  • Varela M, Brás R, Barros IR, Oliveira P, Meierrose C (2008) Opportunity for hybridization between two oak species in mixed stands as monitored by the timing and intensity of pollen production. For Ecol Manag 256:1546–1551

    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 

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Acknowledgments

We would like to thank Andreas Christou (Department of Forests, Republic of Cyprus personnel, for their assistance during plant collections). We are grateful to Mr. Petros Anastasiou for his valuable help during plant collections. 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.

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Correspondence to Charalambos Neophytou.

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Communicated by C. Ammer.

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Neophytou, C., Aravanopoulos, F.A., Fink, S. et al. Interfertile oaks in an island environment. II. Limited hybridization between Quercus alnifolia Poech and Q. coccifera L. in a mixed stand. Eur J Forest Res 130, 623–635 (2011). https://doi.org/10.1007/s10342-010-0454-4

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