Species delimitation in the genus Quercus (Fagaceae)

  • Susana Valencia-A. Facultad de Ciencias, Universidad Nacional Autónoma de México
keywords: criteria to delimiting species, nomenclature, species concepts, taxonomy


Background: Quercus is recognized as a taxonomically complex genus, but also as a model clade in many important fields in biology, such that a good recognition of its species is necessary. The chosen species concept to use in Quercus will determine the empirical criteria used to recognize them, which will impact several areas of knowledge.

Questions: What are the main sources of variation that hinder the delimitation of species in Quercus? What species concepts we use explicitly to recognize species in Quercus? What is the advantage of using different empirical criteria both integrally and simultaneously in delimitation of species of oaks?

Studied species: Species of Quercus

Method: Bibliographic review of the main sources of variation in Quercus, and the species concepts, specifically those used in Quercus.

Results: Plasticity, convergence, hybridization and introgression, and incomplete divergence were identified as the main sources of variation in oaks. Taxonomic and ecological species concepts are those mainly and traditionally used in Quercus. Syngameons are important to know and understand the biology and evolution of Quercus species. These systems indicate that there are preserved genes that provide coherence and morphologic, ecologic and genetic identity to species, even if hybridization, backcrossing and introgression occur.

Conclusions: Preserved genes that provide coherence to species, suggest using taxonomic, ecologic and genetic concepts to delimit problematic species in species complexes in Quercus. The simultaneous use of data that these concepts support (multicriteria analysis), will give more confidence to get closer to the nature of the species and build an integrative taxonomy.


Download data is not yet available.

Author Biography

Susana Valencia-A., Facultad de Ciencias, Universidad Nacional Autónoma de México
Técnico Académico. Herbario de la Facultad de Ciencias, Departamento de Biología Comparada
Species delimitation in the genus <em>Quercus</em> (Fagaceae)


Abbot R, Albach D, Ansell S, Arntze JW, Baird SJE, Bierne N, Joughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK., Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Möst M, Mullen S, Nichols R, Norte AW, Parisod C, Pfennig K, Rice AM, Rithchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26(2): 229-246. DOI: https://doi.org/10.1111/j.1420-9101.2012.02599.x

Abrams MD. 1994. Genotypic and phenotypic variation as stress adaptations in temperate tree species: a review of several case studies. Tree Physiolology 14: 833-842. DOI: https://doi.org/10.1093/treephys/14.7-8-9.833

Aldhebiani AY. 2018. Species concept and specitation. Saudi Journal of Biological Sciences 25: 437-440. DOI: https://doi.org/10.1016/j.sjbs.2017.04.013

Aldrich P, Cavender-Bares J. 2011. Quercus. In: C. Kole (ed.). Wild crop relatives: Genomic and breeding resources, forest trees. Pag. 89-129. Spriger, Berlin. DOI: https://doi.org/10.1007/978-3-642-21250-5_6

Anderson E. 1949. Introgressive hybridization. New York: Wiley & Sons. 109 pp. DOI: https://doi.org/10.5962/bhl.title.4553

Anderson L. 1990. The driving force: species concepts and ecology. Taxon 39(3): 375-382. DOI: https://doi.org/10.2307/1223084

Bacon CD, McKenna MJ, Simmons MP, Wagner WL. 2012. Evaluating multiple criteria for species delimitation: an empirical example using Hawaiian palms (Arecaceae: Prtchardia). BMC Evolutionary Biology 12: 23 DOI: https://www.biomedcentral.com/1471-2148/12/23

Barton NH, Hewitt GM. 1985. Analysis of hybrid zones. Annual Review of Ecology and Systematics. 16: 113-148. DOI: https://doi.org/10.1146/annurev.es.16.110185.000553

Burger WC. 1975. The Species Concept in Quercus. Taxon 24 (1): 45-50. DOI: https://www.jstor.org/stable/10.2307/1218998

Cannon CH, Petit RJ. 2019. The oak syngameon: more than the sum of its parts. New Phytologist 226: 978-983. https://doi.org/10.1111/nph.16091

Cavender-Bares J, Ramírez-Valiente JA. 2017. Physiological evidence from common garden experiments for local adaptation and adaptive plasticity to climate in American live oaks (Quercus section Virentes): implications for conservation under global change. In: Gil-Pelegrín E, Peguero-Pina J, Sancho-Knapik D, eds. Oaks physiological ecology. Exploring the functional diversity of genus Quercus L., Tree Physiology 7. Springer Switzerland, pp. 107-136. ISNN 1568-2544. ISBN 978-3-319-69099-5, ISBN: 978-3-319-69099-5 (eBook). https://doi.org/10.1007/978-3-319-69099-5_4

Cavender-Bares J. 2019. Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution New Phytologist 221: 669-692. DOI: https://doi.org/10.1111/nph.15450

Coyne JA, Orr HA. 2004. Speciation. Sinauer Associaates. Suderland, Massachusetts USA. ISBN: 0-87893-091-4

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

De Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology 56(6): 879-886. DOI: https://doi.org/10.1080/10635150701701083

De Queiroz K. 2011. Branches in the lines of descent: Charles Darwin and the evolution of the species concept. Biological Jorunal of the Linnean Society 103(1): 19-35. DOI: https://doi.org/10.1111/j.1095-8312.2011.01634.x

Eaton DAR, González-Rodríguez A, Hipp A, Cavender-Bares J. 2015. Historical introgression among the American live oaks and the comparative nature of tests for introgression. Evolution 69(10): 2587-2601. DOI: https://doi.org/10.1111/evo.12758

Font-Quer, P. 1963. Diccionario de botánica. Editorial Labor. Barcelona, España. 1244 pp.

Gailing O, Curtu L. 2014. Interspecific gene flow and maintenance of species integrity in oaks. Annals of Forest Research. 57(1):5-18. DOI: https://doi.org/10.15287/afr.2014.171

Grant V. 1981. Plant Speciation. Columbia University Press. USA. 563 pp. ISBN-10: 0231051131

Gugger FF, Cavender-Bares J. 2013. Molecular and morphological support for a Florida origin of the Cuban oak. Journal of Biogeografphy 40: 632-645. https://doi.org/10.1111/j.1365-2699.2011.02610.x

Gutiérrez E, Trejo I. 2014. Efecto del cambio climático en la distribución potencial de cinco especies arbóreas de bosque templado en México. Revista Mexicana de Biodiversidad 85: 179-188. http://dx.doi.org/10.7550/rmb.37737

Hardin JW. 1975. Hybridization and introgression in Quercus alba. Journal of the Arnold Arboretum 56: 336-363.

Harrison RG, Larson EL. 2014. Hybridization, Introgression, and the nature of species Boundaries. Journal of Heredity 105(1): 795-809. https://doi.org/10.1093/jhered/esu033

Hipp AL, Manos PS, González-Rodríguez A, Hahn M, Kaproth M, McVay JD, Valencia Avalos S, Cavender-Bares J. 2018. Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity. New Phytologist 217(1): 439-452. DOI: https://doi.org/10.1111/nph.14773

Hipp AL, Manos PS, Hahn M, Avishai M, Bodénes C, Cavender-Bares J, Crowl, AA, Deng M, Denk T, Fitz-Gibbon S, Gailing O, González-Elizondo MS, González-Rodríguez A, Grimm GW, Jiang X-L, Kremer A, Lesur I, Mcvay JD, Plomion C, Rodríguez-Correa H, Schulze E-D, Simeone MC, Sork VL, Valencia-Avalos S. 2019a. Genomic landscape of the global oak phylogeny. New Phytologist DOI: https://doi.org/10.1111/nph.16162

Hipp AL, Whittemore AT, Garner M, Hahn M, Fitzek E, Guichoux E, Cavender-Bares J, Gugger PF, Manos PS, Pearse IS, Cannon CH. 2019b. Genomic identity of white oak species in an eastern north American syngameon. Annals of the Missouri Botanical Garden 104: 455-477. DOI: https://doi.org/10.3417/2019434

Kusi J, Karsai I. 2020. Plastic leaf morphology in three species of Quercus: The more exposed leaves are smaller, more lobated and denser. Plant Species Biology 35: 24-37. https://doi.org/10.1111/1442-1984.12253

Lee J-H, Jin D-P, Choi B-H. 2014. Genetic differentiation and introgression among Korean evergreen Quercus (Fagaceae) are revealed by microsatellite markers. Annales Boanici Fennici 51: 39-48. DOI: https://doi.org/10.5735/085.051.0105

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

Leroy T, Roux C, Villate L, Bodénès C, Romiguier J, Paiva JAP, Dossat C, Aury JM, Plomion C, Kremer A. 2017. Extensive recent secondary contacts between four European white oak species. New Phytologist. 214: 865-878. https://doi.org/10.1111/nph.14413

Leroy T, Tougemont Q, Dupouey J-L, Bodénès C, Lalanne C, Belser C, Labadie K, Le Provost G, Aury J-M, Kremer A, Plomion C. 2020. Massive postglacial gene flow between European while oaks uncovered genes underlying species barriers. New Phytologist 226: 1183-1197. DOI: https://doi.org/10.1111/nph.16039

Marsico TD, Hellmann JJ, Romero-Severson J. 2009. Patterns of seed dispersal and pollen flow in Quercus garryana (Fagaceae) following post-glacial climatic changes. Journal of Biogeography 36: 929-941. DOI: https://doi.org/10.1111/j.1365-2699.2008.02049.x

Mayden RL. 1997. A hierarchy of species concepts: the denouement in the saga of the species problem. In: Claridge MF, Dawah HA, Wilson M.R. eds. Species: the Units of Biodiversity. Chapman and Hall, London, pp. 381-424.

Mayer E. 1982. The growth of biological thought: diversity, evolution and inheritance. Cambridge, MA: Belknap Press of Harvard University Press. 992 pp. ISBN 9780674364462

Mayr E. 1942 (1999). Systematics and the origin of species from the viewpoint of a zoologist. Harvard University Press, USA. ISBN-10 0674862503

Mishler B, De Luna E. 1997. Sistemática filogenética y el concepto de especie. Boletín de la Sociedad Botánica de México 60: 45-57. DOI: https://doi.org/10.17129/botsci.1518

Muir G, Schlötter 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: https://doi.org/10.1111/j.1365-294X.2004.02418.x

Muller CH. 1942. The Central American species of Quercus. United States Department of Agriculture, Miscellaneous Publication 477. Washington, D.C. 216 pp. https://doi.org/10.5962/bhl.title.65496

Naomi SI. 2011. On the integrated frameworks of species concepts: Mayden´s hierarchy of species concepts and De Queiroz´s unified concept of species. Journal Zoological systematics Evolutionary Research. 49(3): 177-184. DOI: https://doi.org/10.1111/j.1439-0469.2011.00618.x

Neophytou C, Aravanopoulos FA, 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. Forest Ecology and Management 259(10): 2026-2035. DOI: https://doi.org/10.1016/j.foreco.2010.02.013

Nixon KC. 2006. Global and Neotropical distribution and diversity of oak (genus Quercus) and oak forest. In: Kappelle M. ed. Ecology and conservation of neotropical montane oak forest. Ecological Studies (Analysis and Synthesis), 185. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-28909-7_1

Nixon KC, Muller CH. 1993. The Quercus hypoxantha complex (Fagaceae) in northeastern Mexico. Brittonia 45(2): 146-153. DOI: https://www.jstor.org/stable/2807497

Nixon KC, Muller CH. 1997. Quercus Linnaeus sect. Quercus. Flora of North America North of Mexico 3: 471-506. http://floranorthamerica.org/

Ortego J, Gugger PF, Sork VL. 2017. Impacts of human-induced environmental disturbances on hybridization between two ecologically differentiated Californian oak species. New Phytologist 213(2): 942-955. DOI: https://doi.org/10.1111/nph.14182

Palacio-López K, Rodríguez-López N. 2007. Plasticidad fenotípica en Lippia alba (Verbenaceae) en respuesta a la disponibilidad hídrica en dos ambientes lumínicos. Acta Biológica Colobiana 13(1): 187-198.

Peterson AT,. Navarro-Sigüenza AG. 2001. Alternate species concepts as bases for determining priority conservation areas. Conservation Biology 13(2): 427-431. https://doi.org/10.1046/j.1523-1739.1999.013002427.x

Pigliucci M. 2001. Phenotypic plasticity: beyond nature and nurture. Baltimore: The John Hopkins University Press. Baltimore, USA. 328 pp. ISBN 0-8018-6788-6

Pinheiro F, Dantas-Queiroz MV, Palma-Silva C. 2018. Plant species complex as models to understand speciation and evolution: A review of South American studies. Critical Reviews in Plant Sciences 37(1): 54-80. DOI: https://doi.org/10.1080/07352689.2018.1471565

Ramírez-Toro W, Torres-Miranda A, González-Rodríguez A, Ruiz-Sánchez E, Luna-Vega I, Oyama K. 2017. A multicriteria analysis for prioritizing areas for conservation of oaks (Fagaceae: Quercus) in Oaxaca, southern Mexico. Tropical Conservation Sciences 10: 1-29. DOI: https://doi.org/10.1177/1940082917714227

Ramírez-Valiente JA, Sánchez-Gómez D, Aranda I, Valladares F. 2010. Phenotypic plasticity and local adaptation in leaf ecophysiological traits of 13 contrasting cork oak populations under different water availabilities. Tree Physiology 30: 618-627. DOI: https://doi.org/10.1093/treephys/tpq013

Ramírez-Valiente JA, Cavender-Bares J. 2017. Evolutionary trade-offs between drought resistance mechanisms across a precipitation gradient in a seasonally dry tropical oak (Quercus oleoides). Tree Physiology 37(7): 889-901. DOI: https://doi.org/10.1093/treephys/tpx064

Raposo MA, Stopiglia R, Brito GRR, Bockmann FA, Kirwan GM, Gayon J, Dubois A. 2017. What really hampers taxonomy and conservation? A riposte to Garnett and Christidis. Zootaxa 4317(1): 179-184. DOI: 10 https://doi.org/10.11646/zootaxa4317.1.10

Reeves PA, Richards CM. 2011. Species delimitation under the general lineage concept: An empirical example using wild north American hops (Cannabaceae: Humulus lupulus). Systematic Biology 60(1): 45-59. DOI: 10.1093/sysbio/syq056

Rieseberg LH. 1997. Hybrid origins of plant species. Annual Review of Ecology and Systematics 28: 359-389. DOI: https://doi.org/10.1146/annurev.ecolsys.28.1.359

Rieseberg LH, Archer MA, Wayne RK. 1999. Transgressive segregation, adaptation and speciation. Heredity 83: 363-372. DOI: 10.1038/sj.hdy.6886170

Rodríguez-Correa H, Oyama K, Quesada M, Fuchs EJ, Goznález-Rodríguez A. 2018. Contrasting Patterns of Population History and Seed-mediated Gene flow in Two Endemic Costa Rican Oak Species. Journal of Heredity 109(5): 530-542. DOI: https://doi.org/10.1093/jhered/esy011

Romero RS. 2006. Revisión taxonómica del complejo Acutifoliae de Quercus (Fagaceae) con énfasis en su representación en México. Acta Botánica Mexicana 76: 1-45. DOI: https://doi.org/10.21829/abm76.2006.1016

Rosell JA, Olson ME, Weeks A, De-Nova JA, Medina LR, Pérez CJ, Feria TP, Bómez-Bermejo R, Montero JC, Eguiarte LE. 2010. Diversification in species complexes: Test of species origin and delimitation in the Bursera simarouba clade of tropical trees (Burseraceae). Molecular Phylogenetics and Evolution 57: 798-811. DOI: https://doi.org/10.1016/j.ympev.2010.08.004

Ruiz-Sanchez E, Sosa V. 2010. Delimiting species boundaries within the Neotropical bamboo Otatea (Poaceae: Bambusoideae) using molecular, morphological and ecological data. Molecular Phylogenetics and Evolution 54: 344-356. DOI: https://doi.org/10.1016/j.ympev.2009.10.035

Sabás-Rosales JL, Siqueiros ME, Valencia-A S, Enriquez D. E., 2017. Reconocimiento taxonómico de seis especies arbustivas de encinos (Quercus secc. Quercus: Fagaceae) Polibotanica 44: 11-38. DOI: http://dx.doi.org/10.18387/polibotanica.44.2

Sangster G. 2018. Integrative taxonomy of birds: the nature and delimitation of species. In: Tietze DT. ed. Bird Species, Fascinating Life Sciences: Springer Cham, pp. 9-37. https://doi.org/10.1007/978-3-319-91689-7_2

Simeone MC, Piredda R, Papini A, Vesella F, Schirone B. 2013. Application of plastid and nuclear markers to DNA barcoding of Euro-Mediterranean oaks (Querucs, Fagaceae): problems, prospects and phylogenetic implications. Botanical Journal of the Linnean Society 172(4): 478-499. https://doi.org/10.1111/boj.12059

Sites JW Jr, Marshall JC. 2004. Operational criteria for delimiting species. Annual Review of Ecology Evolution and Systematics 35(1): 199-227. DOI: https://doi.org/10.1146/annurev.ecolsys.35.112202.130128

Sork V, Riordan E, Gugger PF, Fitz-Gibbon S, Wei Z, Ortego J. 2016. Phylogeny and introgression of California Scrub whit oaks (Quercus section Quercus). International Oaks 27: 61-74.

Spellenberg, R, Bacon J. 1996. Taxonomy and distribution of a natural group of black oaks of Mexico (Quercus, section Lobatae, subsection Racemiflorae). Systematic Botany 21(1): 85-99 DOI: https://www.jstor.org/stable/2419565

Stace CA. 1978. Breeding systems, variation patterns and species delimitation. In: Street HE. ed. Essays in plant taxonomy, Academic Press. London, England, pp- 57-78

Su X, Wu G, Li L, Liu J. 2015. Species delimitation in plants using the Qinghai-Tibet Plateau endemic Orinus (Poaceae: Tridentinae) as an example. Annals of Botany 116: 35-48. DOI: https://doi.org/10.1093/aob/mcv062

Torres-Miranda A, Luna-Vega I, Oyama K. 2011. Conservation biogeography of red oaks (Quercus, section Lobatae) in Mexico and central America. American Journal of Botany 98: 290-305. DOI: https://doi.org/10.3732/ajb.1000218

Trelease W. 1924. The American oaks. Memoirs of the National Academy of Sciences 20: 1-255. DOI: https://doi.org/10.5962/bhl.title.142965

Valladares F, Chico JM, Aranda I, Balaguer L, Dizengremel P, Manrique E, Dreyer E. 2002. The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees 16: 395-403. https://doi.org/10.1007/s00468-002-0184-4

Valencia-A, S. 2004. Diversidad del género Quercus (Fagaceae) en México. Boletín de la Sociedad Botánica de México 75: 33-53. https://www.redalyc.org/articulo.oa?id=57707503

Valenca-A S, Flores-Franco G, Jiménez-Ramírez J. 2015. A nomenclatural revisión of Quercus acutifolia, Q. conspersa and Q. grahamii (Lobatae, Fagaceae). Phytotaxa 218(3): 289-294. DOI: https://doi.org/10.11646/phytotaxa.218.3.7

Valencia-A S, Sabas R JL, Soto OJ. 2016. A new species of Quercus, section Lobatae (Fagaceae) from the Sierra Madre Oriental, Mexico. Phytotaxa 269(2): 120-126. DOI: https://doi.org/10.11646/phytotaxa.269.2.5

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

VanValen L. 1976. Ecological species, multispecies, and oaks. Taxon 25(2/3): 233-239. DOI: https://doi.org/10.2307/1219444

Vazquez ML, Nixon KC. 2013. Taxonomy of Quercus crassifolia (Fagaceae) and morphologically similar species in Mexico. Brittonia 65(2): 208-227. https://www.jstor.org/stable/24692574

Williams JH, Boecklen WJ, Howard DJ. 2001. Reproductive processes in two oak (Quercus) contact zones with different levels of hybridization. Heredity 87: 680-690. DOI: https://doi.org/10.1046/j.1365-2540.2001.00968.x

Zeng YF, Liao WJ, Petit RJ, Ahang DY. 2010. Explorign Species Limits in Two Closely Related chinese Oaks, PloS One 5(11):e15529. DOI: https://doi.org/10.1371/journal.pone.0015529

How to Cite
Valencia-A., S. (2020). Species delimitation in the genus Quercus (Fagaceae). Botanical Sciences, 99(1), 1-12. https://doi.org/10.17129/botsci.2658