Abstract
Gene flow among closely related species is a not so unusual event, especially in plants. Hybridization and introgression have probably played a relevant role in the evolutionary history of the genus Quercus , for instance in the post-glacial northwards migration of European white oaks. In the same way, hybridization between the Mediterranean sclerophyllous oaks Q. ilex and Q. suber could have been determinant for the survival of the latter species during glaciations. In this chapter, evidences of the ancient introgression between these two species are revised, as well as estimations of current hybridization rates, which are very likely underrated. Pre-zygotic and post-zygotic limitations to introgression between Q. suber and Q. ilex are described. Finally, the effects of hybridization and introgression on cork quality, and the suitability of Q. ilex —Q. suber as a model system for the study of introgression and the maintenance/restoration of species boundaries within the genus are briefly discussed.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Amaral Franco J (1990) Quercus L. In: Castroviejo S et al. (eds) Flora Ibérica 2:15–36
Anderson E (1949) Hybridization of the habitat. Evol 2:1–9
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York, Oxford Series
Arnold ML, Martin NH (2006) Adaptation by introgression. J Biol 8:82
Barberon M, Vermeer JEM, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164:1–13
Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecol Syst 16:113–148
Boavida LC, Varela MC, Feijó J (1999) Sexual reproduction in the cork oak (Quercus suber L.). I. The progamic phase. Sex Plant Reprod 11(6):347–353
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(3):143–152
Bonito A, Varone L, Gratani L (2011) Relationship between acorn size and seedling morphological and physiological traits of Quercus ilex L. from different climates. Photosynthetica 49:75–86
Borzi A (1881) L´llixi-Suergiu (Quercus morisii-Borzi), nuova Querce della Sardegna. Nuov Gior Bot Ital 13(1):3–10
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
Burger W (1975) The species-concept in Quercus. Taxon 24:45–50
Camus A (1936–1954) Les Chênes: monographie du genre Quercus [et Lithocarpus]. Editions Paul Lechevalier, Paris
Castro-Díez P, Montserrat-Martí G (1998) Phenological pattern of fifteen Mediterranean phanerophytes from Quercus ilex communities of NE-Spain. Plant Ecol 139(1):103–112
Cecich RA, Haenche WW (1995) Pollination biology of northern red and black oak. 10th Central Hardwood Forest Conference:238–246
Coelho AC, Lima MB, Neves D, Cravador A (2006) Genetic Diversity of Two Evergreen Oaks [Quercus suber (L.) and Quercus ilex subsp. rotundifolia (Lam.)] in Portugal using AFLP Markers. Silvae Genet 55(3):105–118
Colmeiro M, Boutelou E (1854) Examen de las Encinas y demás arboles de la Peninsula Iberica que producen bellotas, con la designación de los que se llaman mestos. Imprenta de D. Jose M, Geofrin
Díaz M, Møller AP, Pulido FJ (2003) Fruit abortion, developmental selection and developmental stability in Quercus ilex. Oecologia 135:378–385
Díaz-Fernández PM, Climent J, Gil L (2004) Biennial acorn maturation and its relationship with flowering phenology in Iberian populations of Quercus suber. Trees-Struct Funct 18(6):615–621
Díez Morales E (2016) Estudio anatómico de la corteza de los híbridos Quercus ilex x Q. suber. Dissertation, Universidad Politécnica de Madrid
Dodd RS, Rafii ZA (2004) Selection and dispersal in a multispecies oak hybrid zone. Evolution 58:261–269
Ducousso A, Michaud H, Lumaret R (1993) Reproduction and gene flow in the genus Quercus. Ann Sci For 50(S1):91s–106s
Elena-Rosselló JA, de la Cruz PJ (1998) Levels of genetic diversity in natural, mixed populations of oak species. In: Steiner KC (ed.) Diversity and Adaptation in Oak Species. Proceedings of the 2nd meeting of Working Party 2.08.05, Genetics of Quercus, of the IUFRO. University Park, USA
Elena-Rossello JA, Lumaret R, Cabrera E, Michaud H (1992) Evidence for hybridization between sympatric holm-oak and cork oak in Spain based on diagnostic enzyme markers. Vegetatio 99–100:115–118
Eriksson G (2017) Quercus suber—recent genetic research. European Forest Genetic Resources Programme (EUFORGEN), Bioversity International, Rome, Italy
Franke R, Schreiber L (2007) Suberin-a biopolyester forming apoplastic plant interfaces. Curr Opin Plant Biol 10:1–8
Gómez-Casero MT, Galán C, Domínguez-Vilches E (2007) Flowering phenology of Mediterranean Quercus species in different locations (Córdoba, SW Iberian Peninsula). Acta Bot Mal 32:127–146
Govaerts R, Frodin DG (1998) World checklist and bibliography of Fagales (Betulaceae, Corylaceae, Fagaceae and Ticodendraceae). Royal Bot Gardens, London
Graca J, Pereira H (2004) The periderm development in Quercus suber. IAWA J 25:325–335
Gricar J, Jagodic S, Prislan P (2015) Structure and seasonal changes in the bark of sessile oak (Quercus petraea). Trees 29:747–757
Himrane H, Camarero JJ, Gil-Pelegrín E (2004) Morphological and ecophy-siological variation of the hybrid oak Quercus subpyrenaica (Q. faginea x Q. pubescens). Trees 18:566–575
Howard ET (1977) Bark structure of the Southern Upland Oaks. Wood Fiber Sci 9:172–183
Iwasaki M, Takahashi H, Iwakawa H, Nakagawa A, Ishikawa T, Tanaka H, Matsumura Y, Pekker I, Eshed Y, Vial-Pradel S Ito T, Watanabe Y, Ueno Y, Fukazawa H, Kojima S, Machida Y, Machida C (2013) Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis. Development 140:1958–1969
Jato V, Rodríguez-Rajo FJ,·Méndez J, Aira MJ (2002) Phenological behaviour of Quercus in Ourense (NW Spain) and its relationship with the atmospheric pollen season. Int J Biometeorol 46:176–184
Jiménez MP, 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
Joët T, Ourcival JM, Capelli M, Dussert S, Morin X (2016) Explanatory ecological factors for the persistence of desiccation-sensitive seeds in transient soil seed banks: Quercus ilex as a case study. Ann Bot-London 117(1):165–176
Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2002) Plant systematics, a phylogenetic approach. Sinauer Associates, Massachusetts
Kremer A (ed) (2002) Range wide distribution of chloroplast DNA diversity and pollen deposits in European white oaks: inferences about colonisation routes and management of oak genetic resources. For Ecol Manage 156:1–223
Laguna M (1881) Un mesto italiano y varios mestos espanoles. Rev Montes 114:477–486
Llensa de Gelcen S (1943) Sistemática, fitogeografía y utilidad forestal del hibrido x Quercus Morisii Borzi. Anales de la Escuela de peritos agrícolas y superior de agricultura y de los servicios técnicos de agricultura, vol 3. ESAB, Barcelona, pp 315–328
Lodha M, Marco CF, Timmermans MCP (2013) The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev 27:596–601
López de Heredia U, Soto A (2017) Simulation analysis suggest Quercus suber x Quercus ilex hybridization could be underestimated. International Congress on cork oak trees and woodlands—conservation, management, products and challenges for the future, May 25–26, Sassari, Italy
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
López de Heredia U, Carrion JS, Jimenez P, Collada C, Gil L (2007a) Molecular and palaeoecological evidence for multiple glacial refugia for evergreen oaks on the Iberian Peninsula. J Biogeog 34(9):1505–1517
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(4):1209–1220
López de Heredia U, Sánchez H, Soto A (2017a) Molecular evidence of bidirectional introgression between Quercus suber and Quercus ilex. International Congress on cork oak trees and woodlands—conservation, management, products and challenges for the future, May 25–26, Sassari, Italy
López de Heredia U, Duro MJ, Soto A (2017b) Leaf morphology of progenies of Q. suber, Q. ilex, and their hybrids using multivariate and geometric morphometric analysis. International Congress on cork oak trees and woodlands—conservation, management, products and challenges for the future, May 25–26, Sassari, Italy
López-Caamal A, Tovar-Sánchez E (2014) Genetic, morphological, and chemical patterns of plant hybridization. Rev Chil Hist Nat 87:1–14
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-London 96(5):853–861
Machida C, Nakagawa A, Kojima S, Takahashi H, Machida Y (2015) The complex of ASYMMETRIC LEAVES (AS) proteins plays a central role in antagonistic interactions of genes for leaf polarity specification in Arabidopsis WIREs. Dev Biol. 4:655–671
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(24):5259–5266
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20(5):229–237
Matsumura Y, Ohbayashi I, Takahashi H, Kojima S, Ishibashi N, Keta S, Nakagawa A, Hayashi R, Saéz-Vázquez J, Echeverria M, Sugiyama M, Nakamura K, Machida C, Machida Y (2016) A genetic link between epigenetic repressor AS1-AS2 and a putative small subunit processome in leaf polarity establishment of Arabidopsis. Biol Open 5(7):942–954
Miguel A, de Vega-Bartol J, Marum L, Chaves I, Santo T, Leitão J, Varela MC, Miguel CM (2015) Characterization of the cork oak transcriptome dynamics during acorn development. BMC Plant Biol 15:158
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 96:175–184
Montserrat-Martí G, Camarero JJ, Palacio S, Pérez-Rontomé C, Milla R, Albuixech J, Maestro M (2009) Summer-drought constrains the phenology and growth of two coexisting Mediterranean oaks with contrasting leaf habit: implications for their persistence and reproduction. Trees 23(4):787–799
Muller C (1952) Ecological control of hybridization in Quercus: A factor in the mechanism of evolution. Evolution 6:147–161
Natividade JV (1936) Estudo histologico das peridermes do hibrido Quercus ilex X suber, P Cout Publ Dir G Serv Flor III(1)
Ogaya R, Peñuelas J (2004) Phenological patterns of Quercus ilex, Phillyrea latifolia, and Arbutus unedo growing under a field experimental drought. Ecoscience 11(3):263–270
Oliveira P, Custódio AC, Branco C, Reforço I, Rodrigues F, Varela MC, Meierrose C (2003) Hybrids between cork oak and holm oak: isoenzyme analysis. For Genet 10(4):283–297
Pausas JG, Pereira JS, Aronson J (2009) The Tree. In: Aronson J, Pereira JS, Pausas JG (eds) Cork Oak Woodlands on the Edge. Ecology, Adaptive Management and Restoration. Island Press, Washington, USA
Peguero-Pina JJ, Sancho-Knapik D, Barron E, Camarero JJ, Vilagrosa A, Gil-Pelegrín E (2014) Morphological and physiological divergences within Quercus ilex support the existence of different ecotypes depending on climatic dryness. Ann Bot-London 114:301–313
Peñaloza-Ramírez JM, González-Rodríguez A, Mendoza-Cuenca L, Caron H, Kremer A, Oyama K (2010) Interspecific gene flow in a multispecies oak hybrid zone in the Sierra Tarahumara of Mexico. Ann Bot-London 105:389–399
Perea García-Calvo R (2006) Estudio de la estructura de masa de una dehesa de encina con alcornoque en “El Deheson del Encinar” (Toledo). Master Thesis, Universidad Politécnica de Madrid
Perez Rodriguez A (2008) Modelizacion e introgresion en encina y alcornoque: Efecto de los parametros demograficos y adaptativos. Master Thesis, Universidad Politecnica de Madrid
Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A (1997) Chloroplast DNA footprints of postglacial recolonization by oaks. Proc Natl Acad Sci USA 94:9996–10001
Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164
Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246
Potts B, Reid JB (1988) Hybridization as a dispersal mechanism. Evolution 42:1245–1255
Pulido Neves da Costa JS (2011) Differentiation and genetic variability in cork oak populations (Quercus suber L.). Dissertation, Universidade de Lisboa
Quilho T, Sousa V, Tavares F, Pereira H (2013) Bark anatomy and cell size variation in Quercus faginea. Turk J Bot 37:561–570
Rafii ZA, Zavarin E, Pelleau Y (1991) Chemosystematic differentation of Quercus ilex and Q. rotundifolia based on Acorn Fatty Acids. Biochem System Ecol 19(2):163–166
Ramírez-Valiente JA, Valladares F, Gil L, Aranda I (2009) Population differences in juvenile survival under increasing drought are mediated by seed size in cork oak (Quercus suber L.). For Ecol Manage 257:1676–1683
Rieseberg LH (1995) The role of hybridization in evolution: old wine in new skins. Am J Bot 82(7):944–953
Rieseberg LH, Ellstrand NC (1993) What can molecular and morphological markers tell us about plant hybridization? Crit Rev Plant Sci 12:213–241
Rieseberg L, Wendel J (1993) Introgression and its consequences in plants. In: Harrison R (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 70–109
Rieseberg LH, Raymond O, Rosenthal DM et al (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211–1216
Rieseberg LH, Kim S, Randell RA, Whitney KD, Gross BL, Lexer C, Clay K (2007) Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129:149–165
Rushton BS (1993) Natural hybridization within the genus Quercus L. Ann Sci For 50(suppl 1):73s–90s
Salomón R, Lorenzo Z, Valbuena-Carabaña M, Nicolás JL, Gil L (2012) Seed recalcitrant behavior of Iberian Quercus: a multispecies comparison. Aust J For Sci 129(3–4):182–201
Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553
Sen A, Quilho T, Pereira H (2011) Bark anatomy of Quercus cerris L. var. cerris from Turkey. Turk J Bot 35:45–55
Serra O, Hohn C, Franke R, Prat S, Molinas M, Figueras M (2010) A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm. Plant J 62:277–290
Serra O, Chatterjee S, Figueras M, Molinas M, Stark RE (2014) Deconstructing a plant macromolecular assembly: Chemical architecture, molecular flexibility, and mechanical performance of natural and engineered potato suberins. Biomacromolecules 15:799–811
Sever K, Škvorc Z, Bogdan S, Franjić J, Krstonošić D, Alešković I, Kereša S, Fruk G, Jemrić T (2012) In vitro pollen germination and pollen tube growth differences among Quercus robur L. clones in response to meteorological conditions. Grana 51(1):25–34
Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436
Soler M, Serra O, Molinas M, Huguet G, Fluch S, Figueras M (2007) A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol 144:419–431
Soler M, Serra O, Fluch S, Molinas M, Figueras M (2011) Potato skin SSH library yields new candidate genes for suberin biosynthesis and periderm formation. Planta 233:933–945
Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landscape Ecol 21(6):821–836
Soto A, Lorenzo Z, Gil L (2003) Nuclear microsatellite markers for the identification of Quercus ilex L. and Q. suber L. hybrids. Silvae Genet 52(2):63–66
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(6):601–607
Soto A, López de Heredia U, Robledo-Arnuncio JJ, Gil L (2008) Simulation analysis of Quercus ilex-Quercus suber chloroplast introgression. In: Vázquez-Piqué J, Pereira H, González-Pérez A (eds) Suberwood—New challenges for the integration of cork oak forests and products. Universidad de Huelva Publicaciones, Huelva, pp 91–98
Staudt M, Mir C, Joffre R, Rambal S, Bonin A, Landais D, Lumaret R (2004) Isoprenoid emissions of Quercus spp. (Q. suber and Q. ilex) in mixed stands contrasting in interspecific genetic introgression. New Phytol 163:573–584
Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York
Stebbins GL (1974) Flowering plants: evolution above the species level. Belknap Press of Harvard University Press
Trockenbrodt M (1991) Qualitative structural changes during bark development in Quercus robur, Ulmus glabra, Populus tremula and Betula pendula. IAWA Bull 11:141–166
Van Valen L (1976) Ecological species, multispecies, and oaks. Taxon 25:233–239
Varela MC, Valdiviesso T (1996) Phenological phases of Quercus suber L. flowering. For Genet 3:93–102
Varela MC, Bras 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. Forest Ecol Manag 256:1546–1551
Vázquez FM (2013) Micromorphological and Anatomical Characters Used to Differentiate Mediterranean Oaks. J Int Oak Soc 24:122–129
Vazquez FM, Perez MC, Esparrago F, Burzaco A (1993) Hibridos del género Quercus en Extremadura. I Congreso Forestal Español 1:459–465
Vázquez FM, Esparrago F, López-Marquez JA, Jaraquemada F (1992) Flowering of Quercus rotundifolia Lam. In: International workshop quercus ilex l. ecosystems: fuction, dynamics and management. Montpellier-Barcelona, CEPE/CNRS:81
Vázquez FM, Suárez MA, Baselga MP (1996) Nota sobre el efecto de la temperatura y la humedad en la germinación “in vitro” del grano de polen de Quercus rotundifolia Lam., y Q. suber L. Inv Agr Sist Rec. Forest 5(2):351–359
Vázquez FM, Sánchez-Gullón E, Pinto-Gomes C, Pineda MA, García D, Márquez F, Guerra MJ, Blanco J, Vilaviçosa C (2015) Three New Oak Hybrids from Southwest Iberia (Spain and Portugal). J Int Oak Soc 26:43–55
Vila-Viçosa CM, Vázquez FM, Meireles C,·Pinto-Gomes C (2014) Taxonomic peculiarities of marcescent oaks (Quercus) in southern Portugal. Lazaroa 35:139–153
Vitelli M, Vessella F, Cardoni S, Pollegioni P, Denk T, Grimm GW, Simeone MC (2017) Phylogeographic structuring of plastome diversity in Mediterranean oaks (Quercus Group Ilex, Fagaceae). Tree Genet Genomes 13(1):1
Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci USA 88:2540–2544
Yacine A, Bouras F (1997) Self- and cross-pollination effects on pollen tube growth and seed set in Holm oak Quercus ilex L (Fagaceae). Ann Sci For 54(5):447–462
Zhu A, Greaves IK, Dennis ES, Peacock WJ (2017) Genome-wide analyses of four major histone modifications in Arabidopsis hybrids at the germinating seed stage. BMC Genomics 18:137
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
López de Heredia, U., Vázquez, F.M., Soto, Á. (2017). The Role of Hybridization on the Adaptive Potential of Mediterranean Sclerophyllous Oaks: The Case of the Quercus ilex x Q. suber Complex. In: Gil-Pelegrín, E., Peguero-Pina, J., Sancho-Knapik, D. (eds) Oaks Physiological Ecology. Exploring the Functional Diversity of Genus Quercus L.. Tree Physiology, vol 7. Springer, Cham. https://doi.org/10.1007/978-3-319-69099-5_7
Download citation
DOI: https://doi.org/10.1007/978-3-319-69099-5_7
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-69098-8
Online ISBN: 978-3-319-69099-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)