Abstract
Interspecific gene flow between more than two species is a common phenomenon in oaks, which can occur simultaneously among different species, promoting the transfer of genetic material across species boundaries. However, the hybridization dynamics in multispecies hybrid zones remain unknown. In this study, we provide genetic evidence of hybridization and introgression of Quercus castanea across a natural gradient of red oak species richness. We analyzed five populations recognized morphologically as “pure” Q. castanea, one allopatric and four sympatric populations, where the number of red oak species associated with Q. castanea ranged from one to four. Also, one allopatric population of each red oak species that occurs in sympatry with Q. castanea was chosen as reference population (Q. crassipes, Q. laurina, Q. mexicana and Q. crassifolia). In total, six nSSRs were used in 10 and 20 individuals from each allopatric and sympatric populations, respectively. Our results showed that allopatric populations formed completely distinct genetic clusters. In sympatric populations, we found evidence of hybridization and introgression among Q. castanea and three of its associated red oak species. However, the occurrence and frequency of hybrids between Q. castanea and these species varied among stands. Our analyses provide evidence and new insights into hybridization and introgression dynamics within a Mexican red oak species complex, through a focal species, Q. castanea.
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Abadie P, Roussel G, Dencausse B, Bonet C, Bertocchi E, Louvet JM, Kremer A, Garniere 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
Acosta CA (2008) Estructura genética comparada en poblaciones de Quercus castanea y Q. desertícola, en sitios conservados y perturbados en la Cuenca de Cuitzeo, Michoacán, México. B.Sc Dissertation. Universidad Michoacana de San Nicolás de Hidalgo, Michoacán
Albarrán-Lara AL, Mendoza-Cuenca L, Valencia-Avalos S, González-Rodríguez A, Oyama K (2010) Leaf fluctuating asymmetry increases with hybridization and introgression between Quercus magnoliifolia and Quercus resinosa (Fagaceae) through an altitudinal gradient in Mexico. Int J Pl Sci 171:310–322
Aldrich PR, Michler CH, Sun W, Romero-Severson J (2002) Microsatellite markers for northern red oak (Fagaceae: Quercus rubra). Molec Ecol 2:472–474
Aldrich PR, Jagtap M, Michler CH, Romero-Severson J (2003) Amplification of North American red oak microsatellite markers in European white oaks and Chinese chestnut. Silvae Genet 52:176–179
Alvarado-Dávalos LG (2014) Evaluación a escala fina de los efectos de un sistema de tala sobre la viabilidad poblacional de Quercus castanea en la Cuenca del lago Cuitzeo (Michoacán, México). M. Sc Dissertation. Universidad Nacional Autónoma de México, México
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York
Barton NH (2001) The role of hybridization in evolution. Molec Ecol 10:551–568
Boavida LC, Silva JP, Feijó JA (2001) Sexual reproduction in the cork oak (Quercus suber L). II. Crossing intra- and interspecific barriers. Sex Pl Reprod 14:143–152
Buerkle C (2009) Ecological context shapes hybridization dynamics. Molec Ecol 18:2077–2079
Buerkle CA, Rieseberg LH (2001) Low intraspecific variation for genomic isolation between hybridizing sunflower species. Evolution 55:684–691
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 WC (1975) The species concept in Quercus. Taxon 24:45–50
Cavender-Bares J, Pahlich A (2009) Molecular, morphological, and ecological niche differentiation of sympatric sister oak species, Quercus virginiana and Q. geminata (Fagaceae). Amer J Bot 96:1690–1702
Challenger A (1998) Utilización y conservación de los ecosistemas terrestres de México: pasado, presente y futuro. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México
Coyne JA (1994) Ernst Mayr and the origin of species. Evolution 48:19–30
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates Inc, Sunderland
Curtu AL, Gailing O, Finkeldey R (2007) Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evol Biol 7:218
Dodd RS, Afzal-Rafii Z (2004) Selection and dispersal in a multispecies oak hybrid zone. Evolution 58:261–269
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Syst 24:217–242
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molec Ecol 14:2611–2620
Ferrusquía-Villafranca I (1998) Geología de México: una sinopsis. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Diversidad biológica de México: orígenes y distribución. Instituto de Biología, Universidad Nacional Autónoma de México, México
Gómez-Tuena A, Orozco-Esquivel MT, Ferrari L (2007) Expand igneous petrogenesis of 11 the Trans-Mexican Volcanic Belt. Geol Soc Amer Special Pap 22:129–181
González-Rodríguez A, Arias DM, Valencia S, Oyama K (2004) Morphological and RAPD analysis of hybridization between Quercus affinis and Q. laurina (Fagaceae), two Mexican red oaks. Amer J Bot 91:401–409
Guttman SI, Weigt LA (1989) Electrophoretic evidence of relationships among Quercus (oaks) of eastern North America. Canad J Bot 67:339–351
Herrera-Arroyo ML (2013) Efectos de la fragmentación del hábitat en la diversidad y estructura genética de poblaciones de Quercus castanea Née, en la cuenca de Cuitzeo, Michoacán. PhD Dissertation. Universidad Nacional Autónoma de México, Morelia
Himrane H, Camarero JJ, Gil-Pelegrín E (2004) Morphological and ecophysiological variation of the hybrid oak Quercus subpyrenaica (Q. faginea × Q. pubescens). Trees 18:566–575
Howard DJ, Preszler RW, Williams J, Fenchel S, Boecklen WJ (1997) How discrete are oak species? Insights from a hybrid zone between Quercus grisea and Quercus gambelii. Evolution 5:747–755
Jensen J, Larsen A, Nielsen LR, Cottrell J (2009) Hybridization between Quercus robur and Q. petraea in a mixed oak stand in Denmark. Ann Forest Sci 66:706
Kampfer S, Lexer K, Glössl J, Steinkellner H (1998) Characterization of (GA)n microsatellite loci from Quercus robur. Hereditas 129:183–186
Kaplan Z, Fehrer J (2007) Molecular evidence for a natural primary triple hybrid in plants revealed from direct sequencing. Ann Bot (Oxford) 99:1213–1222
Kashani N, Dodd RS (2002) Genetic differentiation of two California red oak species, Quercus parvula var. Shreveii and Q. wislizeni, based on AFLP genetic markers. USDA For Serv Gen Tech Rep 184:417–426
Lagache L, Klein EK, Guichoux E, Petit RJ (2013) Fine-scale environmental control of hybridization in oaks. Molec Ecol 22:423–436
Lepais O, Gerber S (2011) Reproductive patterns shape introgression dynamics and species succession within the European white oak species complex. Evolution 65:156–170
Lepais O, Petit RJ, Guichoux E, Lavabre JE, Alberto F, Kreme A, Gerber S (2009) Species relative abundance and direction of introgression in oaks. Molec Ecol 18:2228–2242
Lepais O, Roussel G, Hubert A, Kremer A, Gerber S (2013) Strength and variability of postmating reproductive isolation barriers between four European white oak species. Tree Genet Genomes 9:841–853
Lexer C, Widmer A (2008) The genic view of plant speciation: recent progress and emerging questions. Phil Trans R Soc B Biol Sci 363:3023–3036
López-Caamal A, Mussali-Galante P, Valencia-Cuevas L, Jiménez Ramírez J, Vega Flores K, Tovar-Sánchez E (2013) Transgressive character expression in hybrid zones between the native invasives Tithonia tubaeformis and Tithonia rotundifolia (Asteraceae) in Mexico. Pl Syst Evol 299:1781–1792
Lowe AJ, Boshier D, Ward M, Bacles CF, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273
Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil Trans R Soc B 363:3009–3021
Moran EV, Willis J, Clark JS (2012) Genetic evidence for hybridization in red oaks (Quercus sect. Lobatae, Fagaceae). Amer J Bot 99:92–100
Muir G, Fleming CC, Schlötterer C (2000) Species status of hybridizing oaks. Nature 405:67–90
Muller C (1952) Ecological control of hybridization in Quercus: a factor in the mechanism of evolution. Evolution 6:147–161
Neophytou C, Dounavi A, Fink S, Aravanopoulos FA (2011) 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
Nixon KC (1993) Infrageneric classification of Quercus (Fagaceae) and typification of sectional names. Ann Sci Forest 50:25s–34s
Olrik D, Kjær ED (2007) The reproductive success of a Q. petraea × Q. robur F1-hybrid in back crossing situations. Ann Forest Sci 64:37–46
Ortego J, Bonal R (2010) Natural hybridization between kermes (Quercus coccifera L.) and holm oaks (Q. ilex L.) revealed by microsatellite markers. Pl Biol 12:234–238
Peñaloza-Ramírez JM (2011) Filogeografía e hibridación de cuatro especies del género Quercus (Fagaceae) en México. PhD. Dissertation. Universidad Nacional Autónoma de México
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 (Oxford) 105:389–399
Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Mcsailkl UM, Van Dam B, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicochea PG, Jensen JS, König AO, Lowe AJ, Flemming S, Mátyás G, Munro RC, Popescu F, Slade D, Tabbener H, de Vries GM, Zeigenhagen B, Beauli JL, Kremer A (2002) Identification of refuge and post-glacial colonization routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol Managem 156:49–74
Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164
Potts BM, Reid JB (1988) Hybridization as a dispersal mechanism. Evolution 42:1245–1255
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rangel SR, Zenteno ECR, Enríquez A (2002) El Género Quercus (Fagaceae) en el Estado de México. Ann Missouri Bot Gard 89:551–593
Rieseberg LH (1997) Hybrid origins of plant species. Ann Rev Ecol Syst 28:359–389
Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914
Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nazakato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211–1216
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Molec Ecol Notes 4:137–138
Rzedowski J, Rzedowski GC (2001) Flora Fanerogámica del Valle de México. Instituto de Ecología, A. C., Centro Regional del Bajío. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México
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. Pl Biol 11:758–765
Sánchez-Ortiz K (2012) Estructura y diversidad genética de Quecus glabrescens a través de un gradiente de encinos blancos asociados. BsSC Dissertation, Universidad Autónoma del Estado de Morelos, México
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207
Steinhoff S (1993) Results of species hybridization with Quercus robur L and Quercus petraea (Matt) Liebl. Ann Sci Forest 50:137–143
Steinkellner H, Fluch S, Turetscheki E, Lexer C, Streiff R, Kremer A, Burg K, Glöss J (1997) Identification and characterization of (GA/CT)n microsatellite loci form Quercus petraea. Pl Molec Biol 33:1093–1096
Templeton AR (1989) The meaning of species and speciation: a genetic perspective. The units of evolution. In: Otte D, Endler JD (eds) Speciation and its consequences. Sinauer, Sunderland
Tovar-Sánchez E, Oyama K (2004) Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico: morphological and molecular evidence. Amer J Bot 91:1352–1363
Vähä JP, Primmer CR (2006) Efficiency of model based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Molec Ecol 15:63–72
Valbuena-Carabana M, González-Martínez SC, Sork VL, Collada C, Soto A, Goicoechea PG, Gil L (2005) Gene flow and hybridisation in a mixed oak forest (Quercus pyrenaica Willd. and Quercus petraea (Matts.) Liebl.) in central Spain. Heredity 95:457–465
Valbuena-Carabana M, González-Martínez SC, Hardy OJ, Gil L (2007) Fine-scale spatial genetic structure in mixed oak stands with different levels of hybridization. Molec Ecol 16:1207–1219
Valencia S (1994) Contribución a la delimitación taxonómica de tres especies del género Quercus subgénero Erythrobalanus: Q. laurina Humboldt et Bonpland, Q. affinis Scheidweiler y Q. ghiesbregthil Martens et Galeotti. MsC Dissertation. Universidad Nacional Autónoma de México, Mexico
Valencia S (1995) Contribución al conocimiento del género Quercus (Fagaceae) en el Estado de Guerrero, México. Contribuciones del Herbario de la Facultad de Ciencias No. 1, Universidad Nacional Autónoma de México, Mexico
Valencia S (2004) Diversidad del género Quercus en México. Bol Soc Bot Mex 75:33–53
Valencia-Cuevas L, Piñero D, Mussali-Galante P, Valencia-Ávalos S, Tovar-Sánchez E (2014) Effect of a red oak species gradient on genetic structure and diversity of Quercus castanea (Fagaceae) in Mexico. Tree Genet Genomes 10:641–652
Van Valen L (1976) Ecological species, multispecies, and oaks. Taxon 25:233–239
Vazquez ML (2006) Trichome morphology in selected Mexican red oak species (Quercus section Lobatae). Sida 22:1091–1110
Williams DG, Ehleringer JR (2000) Carbon isotope discrimination and water relations of oak hybrid populations in southwestern Utah. W N Amer Naturalist 60:121–129
Williams JH, Boecklen WJ, Howard DJ (2001) Reproductive processes in two oak (Quercus) contact zones with different levels of hybridization. Heredity 87:680–690
Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conservation Biol 15:1039–1053
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Acknowledgments
The authors thank Gabriel Flores, Mauricio Mora, Efraín Ramirez, and Guillermo Sánchez for their help with field collections. We also thank Laura Marquez for technical assistance and Tatiana Cervantes for help with the red oaks leaves illustrations. This research was supported by grants from CONACYT- Mexico (61725) to E.T.S. Also, this research was supported by scholarship from CONACYT-SEP Mexico to L.V.C. We also thank the Posgrado en Ciencias Biológicas (UNAM).
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Valencia-Cuevas, L., Mussali-Galante, P., Piñero, D. et al. Hybridization of Quercus castanea (Fagaceae) across a red oak species gradient in Mexico. Plant Syst Evol 301, 1085–1097 (2015). https://doi.org/10.1007/s00606-014-1151-4
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DOI: https://doi.org/10.1007/s00606-014-1151-4