Low genetic differentiation between two morphologically and ecologically distinct giant-leaved Mexican oaks
Quercus magnoliifolia and Q. resinosa are two Mexican white oak species that have been taxonomically reported to exhibit morphological similarities and possible hybridization. The objective of this study was to compare the variation in Q. magnoliifolia and Q. resinosa throughout their distribution range to identify the degree of species differentiation using morphological, ecological and genetic tools. Morphological analysis showed differentiation in leaf shape between the species corresponding to the taxonomical identification of Q. magnoliifolia and Q. resinosa in almost all cases, but intermediate individuals were identified in the middle of the species ranges. Comparison of ecological niche models for Q. magnoliifolia and Q. resinosa showed non-equivalent ecological niches, high climatic niche differences and low to moderate spatial and environmental niche overlap, mainly along the Trans-Mexican Volcanic Belt where morphologically intermediate individuals between species were more frequently located, suggesting recent hybridization by secondary contact. In contrast, we found low but significant genetic differentiation between Q. magnoliifolia and Q. resinosa and lower interspecific than intraspecific genetic differentiation, and Bayesian clustering analysis (K = 2) failed to assign each species to a unique genotype, suggesting shared ancestral variation as the cause of genetic similarity between species due to recent divergence. In conclusion, although neutral molecular markers do not distinguish the species Q. magnoliifolia and Q. resinosa, we found morphological and ecological differentiation between these oaks that provide preliminary evidence for divergent selection.
KeywordsEcological niche Interspecific gene flow Mexican oaks Quercus magnoliifolia Quercus resinosa Species differentiation
We thank the constructive comments and suggestions of two anonymous reviewers to previous drafts. We also thank to V. Rocha, M.D. Lugo-Aquino, N. Pérez-Nasser, A. Palencia for technical assistance; A. Torres-Miranda for ecological niche modelling assistance; S. Valencia for taxonomical identification support; and J. Gonzaga-Espíritu for laboratory assistance.
This work was supported by the graduate programme Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM) and by CONACyT doctoral scholarship  and UC MEXUS—CONACyT postdoctoral fellowship [I010/680/2012; I010/375/2013] to ALAL. This research was supported by DGAPA-PAPIIT (UNAM) [IN209108, IN229803, RV201015], SEMARNAT-CONACyT [2004-311, 2004-C01-97 and 2006-23728], CONACYT  to KO, and by CONACyT-ECOS NORD [grant M03-A01] to AK and KO.
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Conflict of interest
The authors declare that they have no conflict of interest.
The authors comply with all rules of the journal following the COPE guidelines; all authors have contributed and approved the final manuscript.
- 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. https://doi.org/10.1086/650317 CrossRefGoogle Scholar
- Antonecchia G, Fortini P, Lepais O, Gerber S, Léger P, Scippa GS, 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). Ann Forest Res 58:1512. https://doi.org/10.15287/afr.2015.415 CrossRefGoogle Scholar
- Belkhir K, Borsa P, Chikhi L, Raufaste N, Binhomm F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Montpellier: Laboratoire Génome, Populations, interactions, CNRS UMR 5171, Université de Montpellier IIGoogle Scholar
- Broennimann O, Fitzpatrick MC, Pearman PB, Petitpierre B, Pellissier L, Yoccoz NG, Thuiller W, Fortin M-J, Randin C, Zimmermann NE, Graham CH, Guisan A (2012) Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecol Biogeogr 21:481–497. https://doi.org/10.1111/j.1466-8238.2011.00698.x CrossRefGoogle Scholar
- Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package- I: one-table methods. R News 4:5–10Google Scholar
- Curtu AL (2006) Patterns of genetic variation and hybridization in a mixed oak (Quercus spp.) forest. Cuvillier, GöttingenGoogle Scholar
- Development Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Futuyma DJ (2005) Evolution. Sinauer, SunderlandGoogle Scholar
- González-Villarreal LM (1986) Contribuciones al conocimiento del género Quercus en el estado de Jalisco. Colección Flora de Jalisco, Instituto de Botánica, Universidad de Guadalajara, ZapopanGoogle Scholar
- Grant V (1981) Plant speciation. Columbia University Press, New YorkGoogle Scholar
- Hewitt GM (2002) Hybrid zones. In: Pagel M, Godfray C (eds) Encylopedia of evolution. Oxford University Press, New York, pp 552–556Google Scholar
- Jakob SS, Martínez-Meyer E, Blattner FR (2009) Phylogeographic analyses and paleodistribution modeling indicate Pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction. Molec Biol Evol 26:907–923. https://doi.org/10.1093/molbev/msp012 CrossRefPubMedGoogle Scholar
- McVaugh R (1974) Flora Novo-Galiciana. University of Michigan, MichiganGoogle Scholar
- Muller CH, McVaugh R (1972) The oaks (Quercus) described by Née (1801), and by Humboldt and Bonpland (1809), with comments on related species. Contr Univ Michigan Herb 9:507–522Google Scholar
- 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 Quercus robur L.) using small sets of microsatellite markers. Forest Ecol Managem 259:2026–2035. https://doi.org/10.1016/j.foreco.2010.02.013 CrossRefGoogle Scholar
- Phillips SJ, Dudik M, Schapire RE (2004) A maximum entropy approach to species distribution modeling. In: Proceedings of the 21st international conference on machine learning. ACM Press, New York, pp 655–662Google Scholar
- Rohlf FJ (1990) Rotational fit (Procrustes) methods. In: Rohlf FJ, Bookstein F (eds) Proceedings of the Michigan morphometrics workshop. University of Michigan Museums of Zoology, Ann Arbor, pp 227–236Google Scholar
- Rohlf FJ (2005) tpsDig, digitize landmarks and outlines, version 2.04. Department of Ecology and Evolution, State University of New York at Stony Brook, Stony BrookGoogle Scholar
- Rzedowski J (1978) Vegetación de México. Limusa, MéxicoGoogle Scholar
- Salvini D, Bruschi P, Fineschi S, Grossono P, Kjaer 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. https://doi.org/10.1111/j.1438-8677.2008.00158.x CrossRefGoogle Scholar
- Trelease W (1924) The American oaks. Natl Acad Sci 20:1–255Google Scholar
- Valencia S (1994) Contribución a la delimitación taxonómica de tres especies del género Quercus sub. Erytrobalanus. PhD Thesis, Universidad Nacional Autónoma de México, Ciudad de MéxicoGoogle Scholar
- Van Valen L (1976) Ecological species, multispecies and oaks. Taxon 25: 233–239. http://www.jstor.org/stable/1219444
- Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists: a Primer. Elsevier, New YorkGoogle Scholar