Skip to main content

Advertisement

Log in

Effect of a red oak species gradient on genetic structure and diversity of Quercus castanea (Fagaceae) in Mexico

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Incipient reproductive barriers are a common characteristic of oak species. Disruption of these barriers promotes changes in diversity and genetic structure of the species involved. Quercus castanea is a red oak with wide geographic distribution in Mexico, which presents atypically high morphological variability when it occurs in sympatry with other red oak species, suggesting that hybridization may explain the observed variation. We tested if the genetic structure and diversity levels of Q. castanea are related to the number of red oak species growing in sympatry. In total, 14 microsatellite (SSRs) primers (six nSSRs and eight cpSSRs) were used in 120 Q. castanea individuals (20/site) belonging to six populations, where the number of red oak species associated varied from zero to five. Results showed a positive and significant relationship between the genetic diversity of Q. castanea and the number of red oak species growing in sympatry, regardless of the marker type or the parameter of genetic diversity analyzed. Also, we found a higher genetic differentiation of Q. castanea populations using cpSSRs in comparison with nSSRs. Our results suggest that temperate forests with high red oaks species richness co-dominated by Q. castanea promote the increase in this species genetic diversity. From a conservation perspective, high genetic diversity levels of foundation species such as Q. castanea may have positive cascade effects extending to other species in the community.

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

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Adams RI, Goldberry S, Whitham T, Zinkgraf MS, Dirzo R (2011) Hybridization among tree species correlates positively with understory plant diversity. Botany 98:1623–1632

    Article  Google Scholar 

  • Aldrich PR, Michler CH, Sun W, Romero-Severson J (2002) Microsatellite markers for northern red oak (Fagaceae: Quercus rubra). Mol Ecol 2:472–474

    Article  CAS  Google Scholar 

  • Amos W, Worthington J, Fullard K, Burg TM, Croxalli JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc Roy Soc Lond B 268:2021–2028

    Article  CAS  Google Scholar 

  • Anderson E (1949) Introgressive hybridization. Wiley, New York

    Google Scholar 

  • Bacilieri R, Ducousso A, Kremer A (1995) Genetic, morphological and phenological differentiation between Quercus petraea (Matt.) Liebl. and Quercus robur L. in a mixed stand of Northwest of France. Silvae Genet 44:1–10

    Google Scholar 

  • Bailey JP, Schweitzer JA, Rehill BJ, Lindroth RL, Martinsen GD, Whitham TG (2004) Beavers as molecular geneticists: a genetic basis to the foraging of an ecosystem engineer. Ecology 85:603–608

    Article  Google Scholar 

  • Bailey JP, Deckert R, Schweitzer JA, Rehill BJ, Lindroth RL, Gehring C, Whitham TG (2005) Host plant genetics affect hidden ecological players: links among Populus, condensed tannins, and fungal endophyte infection. Can J Bot 83:356–361

    Article  Google Scholar 

  • Bangert JK, Turek RJ, Martinsen GD, Wimp GM, Bailey JK, Whitham TG (2005) Benefits of conservation of plant genetic diversity on arthropod diversity. Conserv Biol 19:379–390

    Article  Google Scholar 

  • Belahbib N, Pemonge M-H, Ouassou A, Sbay H, Kremer A, Petit RJ (2001) Frequent cytoplasmatic exchanges between oaks species that are not closely related: Quercus suber and Q. ilex in Morocco. Mol Ecol 10:2003–2012

    Article  CAS  PubMed  Google Scholar 

  • Bruschi P, Vendramin GG, Bussotti F, Grossoni P (2000) Morphological and molecular differentiation between Quercus petreae (Matt.) Liebl. and Quercus pubescens Willd. (Fagaceae) in Northern and Central Italy. Ann Bot 85:325–333

    Article  Google Scholar 

  • Buggs RJA (2007) Empirical study of hybrid zone movement. Heredity 99:301–312

    Article  CAS  PubMed  Google Scholar 

  • Burgarella C, Lorenzo Z, Jabbour-Zahab R, Lumaret R, Guichoux E, Petit RJ, Soto A, Gill L (2009) Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity 102:442–452

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth M, Morgan MT, Charleswoth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303

    CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Deguilloux MF, 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 

  • Delgado P, Piñero D (2002) Sistemática filogeográfica y sus aplicaciones a la evolución y conservación de los bosques de coníferas en México: el caso de Pinus montezumae y P. pseudostrobus. Acta Universitaria (Guanajuato) 12:3–19

    Google Scholar 

  • Dodd RS, Kashani N (2003) Molecular differentiation and diversity among the California red oaks (Fagaceae; Quercus section Lobatae). Theor Appl Genet 107:884–892

    Article  PubMed  Google Scholar 

  • Dodd RS, Afzal-Rafii Z, Mayer W (2008) Molecular markers show how pollen and seed dispersal affect population genetic structure in Coast Live Oak (Quercus agrifolia Née). In: Standiford RB (ed) Proceedings of the sixth symposium on oak woodlands: today’s challenges, tomorrow’s opportunities. Pacific Southwest Research Station, Forest Service, US Department of Agriculture, Albany

    Google Scholar 

  • Driebe E, Whitham TG (2000) Cottonwood hybridization affects tannin and nitrogen content of leaf litter and alters decomposition. Oecologia 123:99–107

    Article  Google Scholar 

  • Ducousso A, Michaud H, Lumaret R (1993) Reproduction and gene flow in the genus Quercus L. Ann Sci For 50:91–106

    Article  Google Scholar 

  • Duminil J, Fineschi S, Hampe A, Jordano P, Salvini D, Vendramin GG, Petit RJ (2007) Can population genetic structure be predicted from life-history traits? Am Nat 169:662–672

    Article  PubMed  Google Scholar 

  • Dumolin S, Demesure B, Petit RJ (1995) Inherence of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theor Appl Genet 91:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Dutech C, Sork VL, Irwin AJ, Smouse PE, Davis FW (2005) Gene flow and fine-scale genetic structure in a wind-pollinated tree species, Quercus lobata (Fagaceaee). Am J Bot 92:252–261

    Article  CAS  PubMed  Google Scholar 

  • Echt CS, DeVerno L, Anzidei M, Vendramin GG (1998) Chloroplast microsatellites reveal population genetic diversity in red pine, Pinus resinosa Ait. Mol Ecol 7:307–316

    Article  Google Scholar 

  • Ellison A, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Holle BV, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486

    Article  Google Scholar 

  • Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259

    Article  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distance among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • 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. Universidad Nacional Autónoma de México, México, Instituto de Biología, pp 3–108

    Google Scholar 

  • Garant D, Dodson JD, Bernatchez L (2005) Offspring genetic diversity increases fitness of female Atlantic salmon (Salmo salar). Behav Ecol Sociobiol 57:240–244

    Article  Google Scholar 

  • Gómez-Tuena A, Orozco-Esquivel MT, Ferrari L (2007) Expand igneous petrogenesis of the Trans-Mexican Volcanic Belt. Geol Soc Am Spec Pap 22:129–181

    Google Scholar 

  • González-Rodríguez A, Arias DM, Valencia S, Oyama K (2004) Morphological and RAPD analysis of hybridization between Quercus laurina and Quercus affinis (Fagaceae), two Mexican red oaks. Am J Bot 91:401–409

    Article  PubMed  Google Scholar 

  • González-Rodríguez A, Arías DM, Oyama K (2005) Genetic variation of populations within the Quercus affinisQuercus laurina (Fagaceae) complex analyzed with RAPD markers. Can J Bot 83:155–162

    Article  Google Scholar 

  • Govaerts R, Frodin DG (1998) World checklist and bibliography of Fagales (Betulaceae, Corylaceae, Fagaceae and Ticodendraceae). Royal Botanic Gardens, Kew

    Google Scholar 

  • Grivet D, Sork VL, Westfall RD, Davis FW (2008) Conserving the evolutionary potential of California valley oak (Quercus lobata Née): a multivariate approach to conservation planning. Mol Ecol 17:139–156

    Article  PubMed  Google Scholar 

  • Guttman SI, Weight LA (1989) Electrophoretic evidence of relationships among Quercus (oaks) of eastern North America. Can J Bot 67:339–351

    Article  Google Scholar 

  • Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown ADH, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding and genetic resources. Sinauer, Sunderland, pp 43–63

    Google Scholar 

  • Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plan species. New Forest 6:95–124

    Article  Google Scholar 

  • Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hersch EI, Roy BA (2007) Context-dependent pollinator behavior: an explanation for patterns of hybridization among three species of Indian paintbrush. Evolution 61:111–124

    Article  PubMed  Google Scholar 

  • Heuertz M, Ois Hausman J-F, Hardy OJ, Vendramin GG, Frascaria-Lacoste N, Vekemans X (2004) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution 58:976–988

    PubMed  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Himrane H, Camarero JJ, Gil-Pelegrín E (2004) Morphological and ecophysiological variation of the hybrid oak Quercus subpyrenaica (Q. faginea × Q. pubescens). Trees-Struct Funct 18:566–575

    Article  Google Scholar 

  • Iason GR, Lennon JJ, Pakeman RJ, Thoss V, Beaton JK, Sim DA, Elston DA (2005) Does chemical composition of individual Scots pine trees determine the biodiversity of their associated ground vegetation? Ecol Lett 8:364–369

    Article  Google Scholar 

  • Ishida TA, Hattori K, Sato H, Kimura MT (2003) Differentiation and hybridization between Quercus crispula and Q. dentata (Fagaceae): insights from morphological traits, amplified fragment length polymorphism markers, and leafminer composition. Am J Bot 90:769–776

    Article  PubMed  Google Scholar 

  • Jensen J, Larsen A, Nielsen LR, Cottrell J (2009) Hybridization between Quercus robur and Q. petraea in a mixed oak stand in Denmark. Ann For Sci 66:1–12

    Article  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 K, Glössl J, Steinkellner H (1998) Characterization of (GA)n microsatellite loci from Quercus robur. Hereditas 129:183–186

    Article  CAS  Google Scholar 

  • Kremer A, Petit RJ (1993) Gene diversity in natural populations of oak species. Ann Sci For 50:186–202

    Article  Google Scholar 

  • Kremer A, Petit R, Zanetto A, Fougère V, Ducousso A, Wagner D, Chauvin C (1991) Nuclear and organelle gene diversity in Q. robur and Q. petraea. In: Ziehe M, Müller-Starck G (eds) Genetic variation of forest tree populations in Europe. Sauerländer, Frankfurt-Am-Main, pp 141–146

    Google Scholar 

  • Lagache L, Klein EK, Guichoux E, Petit R (2013) Fine-scale environmental control of hybridization in oaks. Mol Ecol 22:423–436

    Google Scholar 

  • Lahtinen MJ, Pulkkinen P, Helander ML (1996) Potential gene flow by pollen between English oak (Quercus robur L.) stands in Finland. For Stud 28:47–50

    Google Scholar 

  • Lamont BB, He T, Enright NJ, Krauss SL, Miller BP (2003) Anthropogenic disturbance promotes hybridization between Banksia species by altering their biology. J Evol Biol 16:551–557

    Article  CAS  PubMed  Google Scholar 

  • Le Corre V, Dumolin-Lapègue S, Kremer A (1997) Genetic variation at allozyme and RAPD loci in sessile oak Quercus petreae (Matt.) Liebl. The role of history and geography. Mol Ecol 6:519–529

    Article  Google Scholar 

  • Le Corre V, Roussel G, Zanneto A, Kremer A (1998) Geographical structure of gene diversity in Q. petreae (Matt) Liebl. III. Patterns of variation identified by geostatistical analysis. Heredity 80:464–473

    Article  Google Scholar 

  • 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

    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  CAS  PubMed  Google Scholar 

  • Levin DA (1981) Dispersal versus gene flow in plants. Ann Mo Bot Gard 68:233–253

    Article  Google Scholar 

  • Lorenzo Z, Burgarella C, López de Heredia U, 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 Central  PubMed  Google Scholar 

  • Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Ann Rev Ecol Syst 15:65–95

    Article  Google Scholar 

  • Lowe A, Harris S, Ashton P (2004) Ecological genetics: design, analysis and application. Blackwell, UK

    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  CAS  PubMed Central  PubMed  Google Scholar 

  • Mariette S, Cottrell J, Csaikl UM, Goikoechea P, König A, Lowe AJ, Van Dam BC, Barreneche T, Bodénès C, Streiff R, Burg K, Groppe K, Munro RC, Tabbener H, Kremer A (2002) Comparison of levels of genetic diversity detected with AFLP and microsatellite markers within and among mixed Q. petraea (MATT.) Liebl. and Q. robur L. stands. Silvae Genet 51:72–79

    Google Scholar 

  • McCauley RA, Cortés-Palomec AC, Oyama K (2007) Phylogeography and historical gene flow patterns in disjunctive Quercus across the Sierra Madre Occidental and Southern Cordillera of Mexico. Bot Soc Amer Plant Biol, Chicago. Available at http://www.2007.botanyconference.org/engine/search/index.php

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

    Google Scholar 

  • Nixon KC (1993) The genus Quercus in Mexico. In: Nixon KC (ed) Biological diversity of Mexico, origins and distribution. Oxford University Press, New York, pp 447–458

    Google Scholar 

  • Peñaloza-Ramírez JM (2011) Filogeografía e hibridación de cuatro especies del género Quercus (Fagaceae). Dissertation, Universidad Nacional Autónoma de México

  • Peñaloza-Ramírez JM, González-Rodríguez A, Mendoza-Cuenca A, Caron H, Kremer A, Oyama K (2010) Interspecific gene flow in a multispecies oak hybrid zone in the Sierra Tarahumara of Mexico. Ann Bot 105:389–399

    Article  PubMed Central  PubMed  Google Scholar 

  • Petit RJ, Kremer A, Wagner DB (1993) Geographic structure of chloroplast DNA polymorphisms in European oaks. Theor Appl Genet 87:122–128

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, Latouche-Hallé C, Pemonge MH, Kremer A (2002a) Chloroplast DNA variation of oaks in France and the influence of forest fragmentation on genetic diversity. For Ecol Manag 156:115–129

    Article  Google Scholar 

  • Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cotrell J, Csaikl UM, van Dam BC, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicochea PG, Jenses JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Popescu F, Slade D, Tabberner H, de Vries SMG, Ziegenhagen B, de Beaulieu JL, Kremer A (2002b) Identification of refugia and post-glacial colonization routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manag 156:49–74

    Article  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brever S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Stack G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin G (2003) Glacial refugia: hotspots but no melting pots of genetic diversity. Science 300:1563–1565

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, Bodénès 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  CAS  PubMed  Google Scholar 

  • Queller DG, Goodnight KE (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (v 1.2): population genetics software for exact tests and ecumenicism. J Hered 89:248–249

    Google Scholar 

  • Rieseberg LH, Carney SE (1998) Plant hybridization. New Phytol 140:599–624

    Article  Google Scholar 

  • Rieseberg LH, Wendell JF (1993) Introgression and its consequences in plants. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 70–109

    Google Scholar 

  • 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

  • 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

  • Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA (1998) Philogeographic studies in plants: problems and prospects. Mol Ecol 7:465–474

    Article  Google Scholar 

  • Schoen DJ, Brown DHA (1991) Intraspecific variation in population gene diversity and effective populations size correlates with the mating system in plants. Proc Natl Acad Sci U S A 88:4494–4497

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Spellenberg R (1995) On the hybrid nature of Quercus basaseachicensis (Fagaceae: Sect. Quercus). Sida 16:427–437

    Google Scholar 

  • Statsoft INC (2007) STATISTICA for windows. Tulsa, USA

    Google Scholar 

  • 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 from Quercus petraea. Plant Mol Biol 33:1093–1096

    Article  CAS  PubMed  Google Scholar 

  • Streiff R, Labbe T, Baculieri R, Steinkellner H, Glössl J, Kremer A (1998) Within-population genetic structure in Quercus robur L. and Quercus petraea (Matt.) Liebl. assessed with isozymes and microsatellites. Mol Ecol 7:317–328

    Article  Google Scholar 

  • Tovar-Sánchez E, Oyama K (2004) Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico: morphological and molecular evidence. Am J Bot 91:1352–1363

    Article  PubMed  Google Scholar 

  • Tovar-Sánchez E, Oyama K (2006) Effect of hybridization of the Quercus crassifolia × Quercus crassipes complex on the community structure on endophagous insects. Oecologia 147:702–713

    Article  PubMed  Google Scholar 

  • Tovar-Sánchez E, Mussali-Galante P, Esteban-Jiménez R, Piñero D, Arias DM, Dorado O, Oyama K (2008) Chloroplast DNA polymorphism reveals geographic structure and introgression in the Quercus crassipes × Quercus crassifolia hybrid complex in Mexico. Botany 86:228–239

    Article  Google Scholar 

  • Valbuena-Carabaña M, González-Matínez SC, Sork VL, Collada C, Soto A, Goicochea PG (2005) Gene flow and hybridization in a mixed oak forest (Quercus pyrenaica Willd. and Quercus petraea (Matts.) Liebl.) in central Spain. Heredity 95:457–465

    Article  PubMed  Google Scholar 

  • Valbuena-Carabaña M, González-Martínez SC, Hardy OJ, Gil L (2007) Fine-scale spatial genetic structure in mixed oak stands with different levels of hybridization. Mol Ecol 16:1207–1219

    Article  PubMed  Google Scholar 

  • 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

  • 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, México, D.F.

  • Valencia S (2004) Diversidad del género Quercus en México. Bol Soc Bot Méx 75:33–53

    Google Scholar 

  • Vázquez ML (2006) Trichome morphology in selected Mexican red oak species (Quercus section Lobatae). Sida 22:1091–1110

    Google Scholar 

  • Weir BS (1996) Genetic data analysis II. Sinauer, Sunderland

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Whitham TG, Bailey JK, Scheweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DC, Gehrig CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nature 7:510–523

    CAS  Google Scholar 

  • Williams DG, Ehleringer JR (2000) Carbon isotope discrimination and water relations of oak hybrid populations in southwestern Utah. West N Am Nat 60:121–129

    Google Scholar 

  • Williams JH, Williams JB, Howard DJ (2001) Reproductive processes in two oak (Quercus) contact zones with different levels of hybridization. Heredity 87:680–690

    Article  CAS  PubMed  Google Scholar 

  • Wimp GM, Young PW, Woolbright SA, Martinsen GD, Keim P, Whitham TG (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7:776–780

    Article  Google Scholar 

  • Yeh FC, Boyle T, Rongcai Y, Ye Z, Xian JM (1999) POPGENE, Version 1.31. A Microsoft Window based freeware for population genetic analysis. University of Alberta, Edmonton

  • Zar JH (2010) Biostatistical analysis. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Zeng Y-F, Liao W-J, Petit RJ, Zhang D-Y (2010) Exploring species limits in two closely related Chinese oaks. PLoS ONE 5:e15529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Gabriel Flores, Mauricio Mora, Efraín Ramírez, and Guillermo Sánchez for their help with field collections and Guadalupe Rangel and Laura Marquez for technical assistance. 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). This paper is a requirement to obtain the Ph.D. of L.V.C.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Efraín Tovar-Sánchez.

Additional information

Communicated by A. Kremer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valencia-Cuevas, L., Piñero, D., Mussali-Galante, P. et al. Effect of a red oak species gradient on genetic structure and diversity of Quercus castanea (Fagaceae) in Mexico. Tree Genetics & Genomes 10, 641–652 (2014). https://doi.org/10.1007/s11295-014-0710-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-014-0710-8

Keywords

Navigation