Research article

DOI: 10.15287/afr.2015.415

Genetic structure of a natural oak community in central Italy: Evidence of gene flow between three sympatric white oak species (Quercus, Fagaceae)

Gaby Antonecchia, Paola Fortini, Olivier Lepais, Sophie Gerber, Patrick Legér, Gabriella Stefania Scippa, Vincenzo Viscosi

Gaby Antonecchia
Università degli Studi del Molise, Cda Fonte Lappone IT-86070 Pesche, Italia
Paola Fortini
Università degli Studi del Molise, Cda Fonte Lappone IT-86070 Pesche, Italia
Olivier Lepais
INRA, UMR 1224 ECOBIOP, F-64310 Saint Pée sur Nivelle, France, Université Pau and Pays Adour, UMR 1224 ECOBIOP, F-64600 Anglet, France
Sophie Gerber
INRA, UMR 1202 BIOGECO, 69 route d’Arcachon, F-33612 Cestas cedex, France, Université de Bordeaux, F-33612 Cestas cedex, France
Patrick Legér
INRA, UMR 1202 BIOGECO, 69 route d’Arcachon, F-33612 Cestas cedex, France
Gabriella Stefania Scippa
Università degli Studi del Molise, Cda Fonte Lappone IT-86070 Pesche, Italia
Vincenzo Viscosi
MIUR, Department for Instruction, Institute “O. D’Uva”, IT-86090 Castelpetroso, Italy. Email: vincenzo.viscosi@istruzione.it

Online First: July 20, 2015
Antonecchia, G., Fortini, P., Lepais, O., Gerber, S., Legér, P., Scippa, G., Viscosi, V. 2015. Genetic structure of a natural oak community in central Italy: Evidence of gene flow between three sympatric white oak species (Quercus, Fagaceae). Annals of Forest Research DOI:10.15287/afr.2015.415


Incomplete reproductive barriers between species, especially in sympatric areas where several species coexist, may result in hybridization and an increase in genetic diversity. Here we assessed the amount of genetic diversity in a community of three interfertile and sympatric European oaks (Quercus frainetto Ten., Q. petraea Liebl. Matt. and Q. pubescens Willd.) situated in central Italy. We used 11 microsatellite markers derived from Expressed Sequence Tag (EST-SSRs) and we implemented a Bayesian clustering analysis to assign individuals to species or hybrids. All genotyped loci were polymorphic for all the species and three genetic clusters corresponding to each species were detected. Significant differences and a higher level of gene flow were observed between the three oak species. Occurrence of hybrids varied markedly within the studied area: hybrids between Q. petraea and Q, pubescens were the most frequent, while hybrids between Q. petraea and Q. frainetto were particularly rare. Q. pubescens and Q. petraea showed the highest number of alleles compared to Q. frainetto,which was characterized by a low number of private, but highly frequent, alleles. However, Q. frainetto showed a lower genetic diversity and a stronger reproductive isolation from the other two oak species.


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.). Journal of Evolutionary Biology 25: 157-173. DOI: 10.1111/j.1420-9101.2011.02414.x

Bacilieri R., Ducousso A., Kremer A., 1995. Genetic, morphological, ecological and phenological differentiation between Quercus petraea (Matt.) Liebl. and Quercus robur L. in a mixed stand of northwest ofFrance. Silvae Genetica 44: 1-9.

Brewer S., Cheddadi R., De Beaulieu J., Reille M., 2002. The spread of deciduous Quercus throughout Europesince the last glacial period. ForestEcology and Management 156: 27-48. DOI: 10.1016/S0378-1127(01)00646-6

Campana M.G., Hunt H.V., Jones H., White J., 2010. CorrSieve: software for summarizing and evaluating Structure. Molecular Ecology Resources 11: 349-352. DOI: 10.1111/j.1755-0998.2010.02917.x

Curtu A.L., Gailing O., Finkeldey R., 2007. Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evolutionary Biology 7: 218-233. DOI: 10.1186/1471-2148-7-218

Curtu A.L., Gailing O., Leinemann L., Finkeldey R., 2007b. Genetic variation and differentiation within a natural community of five oak species (Quercus spp.). Plant Biology 9: 116-126. DOI: 10.1055/s-2006-924542

Curtu A.L., Moldovan I.C., Enescu C.M., Craciunesc I., Sofletea N., 2011. Genetic differentiation between Quercus frainetto Ten and Q. pubescens Willd. inRomania. Notulae Botanicae Horti AgrobotaniciCluj-Napoca39(1): 275-282.

Curtu A.L., Craciunesc I., Enescu C.M., Vidalis A., Sofletea N., 2015. Fine-scale spatial genetic structure in a multi-oak-species (Quercus spp.) forest. iForest (early view): e1-e9 [online 2014-09-05] URL: http://www.sisef.it/iforest/contents/?id=ifor1150-008.

Di Pietro R., Viscosi V., Peruzzi L., Fortini P.,2012. Areview of the application of the name Quercus dalechampii. Taxon 61: 1311-1316.

Duminil J., Caron H., Scotti I., Cazal S.O., Petit R.J., 2006. Blind population genetics survey of tropical rainforest trees. Molecular Ecology 15: 3505-3513. DOI: 10.1111/j.1365-294X.2006.03040.x

Durand J., Bodénès C., Chancerel E. et al., 2010. Afast and cost-effective approach to develop and map EST-SSR markers: oak as a case study. Genomic 11:570-583. DOI: 10.1186/1471-2164-11-570

Dzialuk A., ChybickiI., Burczyk J., 2005. PCR multiplexing of nuclear microsatellite loci in Quercus species. Plant Molecular Biology Reporter 23: 121-128. DOI: 10.1007/BF02772702

Evanno G., Regnaut S., Goudet J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611-2620. DOI: 10.1111/j.1365-294X.2005.02553.x

Falush D., Stephens M., Pritchard J.K., 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.

Fortini P., Viscosi V., Fineschi S., Vendramin G.G., 2009. Comparative leaf surface morphology and molecular data of five oaks of subgenus Quercus Oerst. (Fagaceae). Plant Biosystems 143: 543-554. DOI: 10.1080/11263500902722980

Fortini P., Antonecchia G., Di Marzio P., Maiuro L., Viscosi V., 2013. Role of micromorphological leaf traits and molecular data in taxonomy of three sympatric white oak species and their hybrids (Quercus L.). DOI: 10.1080/11263504.2013.868374. DOI: 10.1080/11263504.2013.868374

Gerber S., Chadoeuf J., Gugerli F., Lascoux M., Buiteveld J., Cottrell J., Dounavi A., Fineschi S., Forrest L.L., Fogelqvist J., Goicoechea P.G., Jensen J.S., Salvini D., Vendramin G.G., Kremer A., 2014. High rates of gene flow by pollen and seed in oak populations across Europe. PlosOne 9(1): e85130. DOI: 10.1371/journal.pone.0085130

Goudet J., 2001. FSTAT, a Program to Estimate and Test Gene Diversities and Fixation Indices Version 2.9.3. 2001. URL: http://www2.unil.ch/popgen/softwares/fstat.htm (09 April 2014)

Gugerli F., Walser J.C., 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. Annals of Botany 99: 713-722. DOI: 10.1093/aob/ mcm006

Guichoux E., P. Garnier-Géré, L. Lagache, T. Lang, C. Boury, R.J. Petit, 2013 : Outlier loci highlight the direction of introgression in oaks. Molecular Ecology 22:450-462. DOI: 10.1111/ mec.12125

Guichoux E., Lagache L., Wagner S., Chaumeil P., Léger P., Lepais O., Lepoittevein C., Malausa T., Revardel E., Salin F., Petit R.J., 2011a. Current trends in microsatellite genotyping. Molecular Ecology Resources 11: 591-611. DOI: 10.1111/j.1755-0998.2011.03014.x

Guichoux E.,Lagache L., Wagner S., Léger P., Petit R.J., 2011b. Two highly validated multiplexes (12-plex and 8-plex) for species delimitation and parentage analysis in oaks (Quercus spp.). Molecular Ecology Resources 11: 578-585. DOI: 10.1111/j.1755-0998.2011.02983.x

Guichoux E., Garnier-Géré P., Lagache L., Lang T., Boury C., Petit R.J., 2013. Outlier loci highlight the direction of introgression in oaks. Molecular Ecology 22: 450-462. DOI: 10.1111/mec.12125

Lagache L., E.K. Klein, E. Guichoux, R.J. Petit, 2013: Fine-scale environmental control of hybridization in oaks. Molecular Ecology 22: 423-436. DOI: 10.1111/mec.12121

Lepais O., Léger P., Gerber S., 2006. Short Note: High Throughput Microsatellite Genotyping in Oak Species. Silvae Genetica 55: 4-5.

Lepais O., Petit R.J., Guichoux E., Lavabre J.E., Alberto F., Kremer A., Gerber S., 2009. Species relative abundance and direction of introgression in oaks. Molecular Ecology 18: 2228-2242. DOI: 10.1111/j.1365-294X.2009.04137.x

Lepais O., Gerber S., 2011. Reproductive patterns shape introgression dynamics and species succession within the European white oak species complex. Evolution 65-1: 156-170.

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 Genetics and Genomes 9: 841-853. DOI: 10.1007/s11295-013-0602-3

Lind J.F., Gailing O., 2013. Genetic structure of Quercus rubra L. and Quercus ellipsoidalis E. J. Hill populations at gene-based EST-SSR and nuclear SSR markers. Tree Genetics and Genomes 3: 707-722. DOI: 10.1007/s11295-012-0586-4

Lòpez de Heredia U., Valbuena-Carabana M., Còrdoba M., Gil L., 2009. Variation components in leaf morphology of recruits of two hybridising oaks [Q. petraea (Matt.) Liebl. and Q. pyrenaica Willd.] at small spatial scale. European Journal of ForestResources 128: 543-554. DOI: 10.1007/s10342-009-0302-6

Mucina L., Schaminée J.H.J., Rodwell J., 2000. Common data standards for recording relevés in field survey for vegetation classification. Journal of Vegetation Science 11: 769-772. DOI: 10.2307/3236581

Muir G., Schlötterer C., 2005. Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Molecular Ecology 14: 549-561. DOI: 10.1111/j.1365-294X.2004.02418.x

Neophytou C., Aravanopoulos F.A., Fink S., Dounavi A., 2010. 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. ForestEcology and Management 259: 2026-2035. DOI: 10.1016/j.foreco.2010.02.013

Nixon K.C., 1993. Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. Annals of ForestScience 50: 25-34. DOI: 10.1051/forest:19930701

Peakall R., Smouse P., 2006. GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288-295. DOI: 10.1111/ j.1471-8286.2005.01155.x

Petit R.J., El Mousadik A., Pons O., 1998. Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12: 844-855. DOI: 10.1046/j.1523-1739.1998. 96489.x

Petit R.J., Aguinagalde I., de Beaulieu J.L., Bittkau C., Brewer S., Cheddadi R., Ennos R., Fineschi S., Grivet D., Lascoux M., Mohanty A., Müller-Starck G., Demesure-Musch B., Palmé A., Martín J.P., Rendell S., Vendramin G.G., 2003. Glacial Refugia: Hotspots But Not Melting Pots of Genetic Diversity. Science 300: 1563-1565.
DOI: 10.1126/science.1083264

Pritchard J.K., Stephens M., Donnelly P., 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.

Rieseberg L.H., 1997. Hybrid origins of plant species. Annual Review of Ecology, Evolution, and Systematics 28: 359-389. DOI: 10.1146/annurev.ecolsys.28.1.359

Rushton B.S., 1983. An analysis of variation of leaf characters in Quercus robur L. and Quercus petraea (Matt.) Liebl. population samples fromNorthern Ireland. Irish Forestry 40: 52-77

Salvini D., Bruschi P., Fineschi S., Grossoni P., Kjaer E.D., Vendramin G.G., 2009. Natural hybridisation between Quercus petraea (Matt.) Liebl. And Quercus pubescens Willd. Within an Italian stand as revealed by microsatellite fingerprinting. Plant Biology 11: 758-765. DOI: 10.1111/j.1438-8677.2008.00158.x

Schwarz O. 1993. Quercus L. In Tutin T.G., Burges N.A.,Chater A.O., Edmondson J.R., Heywood V.H., Moore D.M., Valentine D.H., Walters S.M., Webb D.A. (eds.). Flora Europaea.CambridgeUniversityPress,Cambridge, Vol. 1: 72–76.

Toonen R.J., Hughes S., 2001. Increased Throughput for Fragment Analysis on ABI Prism 377 Automated Sequencer Using a Membrane Comb andSTRandSoftware. Biotechniques 31: 1320-1324.

Tovar-Sánchez E., Oyama K., 2004. Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico: morphological and molecular evidence. American Journal of Botany 91: 1352-1363. DOI: 10.3732/ajb.91.9.1352

Valbuena-Caraba-a M., Gonzalez-Martinez S.C., Sork V.L., Collada C., Soto A., Goicoechea P.G., Gil L., 2005. Gene flow and hybridisation in a mixed oak forest (Quercus pyrenaica Wild. And Quercus petraea (Matts.) Liebl.) in central Spain. Heredity 95: 457-465. DOI: 10.1038/ sj.hdy.6800752

Valbuena-Caraba-a M., González-MartínezS.C., Hardy O.J., Gil L., 2007. Fine-scale spatial genetic structure in mixed oak stands with different levels of hybridization. Molecular Ecology 16: 1207-1219.
DOI: 10.1111/j.1365-294X.2007.03231.x

Van Oosterhout C., Hutchinson W.F., Wills D.P., Shipley P., 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535-538. DOI: 10.1111/j.1471-8286.2004.00684.x

Viscosi V., Lepais O., Gerber S., Fortini P., 2009. Leaf morphological analysis in four European oak species (Quercus) and their hybrids: a comparison of traditional and new morphometric methods. Plant Biosystems 143: 564-574. DOI: 10.1080/11263500902723129

Viscosi V., Fortini P., 2011. Leaf shape variation and differentiation in three sympatric white oak species revealed by elliptic Fourier analysis. Nordic Journal of Botany 29: 632-640. DOI: 10.1111/j.1756-1051.2011.01098.x

Viscosi V., Antonecchia G., Lepais O., Fortini P., Gerber S., Loy A., 2012. Leaf shape and size differentiation in white oaks: assessment of allometric relationships among three sympatric species and their hybrids. International Journal of Plant Sciences 173: 875-884. DOI: 10. 1086/667234

Williams J.H., Boecklen W.J., Howard D.J., 2001. Reproductive processes in two oak (Quercus) contact zones with different levels of hybridization. Heredity 87: 680-690. DOI: 10.1046/j.1365-2540.2001.00968.x


Supplementary Data
| DOWNLOAD 80KB
No metrics available for this article.