Abstract
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.
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References
Abbott RJ (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405. https://doi.org/10.1016/0169-5347(92)90020-C
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
Aldrich PR, Michler CH, Sun W, Romero-Severson J (2002) Microsatellite markers for northern red oak (Fagaceae: Quercus rubra). Molec Ecol Notes 2:472–474. https://doi.org/10.1046/j.1471-8278.2002.OM82x
Aldrich PR, Parker GR, Michler CH, Romero-Severson J (2003) Whole-tree silvic identifications and the microsatellite genetic structure of a red oak species complex in an Indiana old-growth forest. Canad J Forest Res 33:2228–2237. https://doi.org/10.1139/X03-160
Anderson RP, Lew D, Peterson AT (2003) Evaluating predictive models of species distributions: criteria for selecting optimal models. Ecol Model 162:211–232. https://doi.org/10.1016/S0304-3800(02)00349-6
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
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 II
Bickford D, Lohman DJ, Sohdi NS, Ng PKI, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155. https://doi.org/10.1016/j.tree.2006.11.004
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
Bruschi P, Vendramin GG, Bussotti F, Grossoni P (2000) Morphological and molecular differentiation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. (Fagaceae) in Northern and Central Italy. Ann Bot (Oxford) 85:325–333. https://doi.org/10.1006/anbo.1999.104
Burger WC (1975) The species concept in Quercus. Taxon 24:45–50. https://doi.org/10.2307/1218998
Campana MG, Hunt HV, Jones H, White J (2011) CorrSieve: software for summarizing and evaluating structure output. Molec Ecol Res 11:349–352. https://doi.org/10.1111/j.1755-0998.2010.02917.x
Chapman MA, Hiscock SJ, Filatov DA (2013) Genomic divergence during speciation driven by adaptation to altitude. Molec Biol Evol 30:2553–2567. https://doi.org/10.1093/molbev/mst168
Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package- I: one-table methods. R News 4:5–10
Cooper EA, Whittall JB, Hodges SA, Nordborg M (2010) Genetic variation at nuclear loci fails to distinguish two morphologically distinct species of Aquilegia. PLoS ONE 5:e8655. https://doi.org/10.1371/journal.pone.0008655
Craft KJ, Ashley MV (2006) Population differentiation among three species of white oak in northeastern Illinois. Canad J Forest Res 36:206–215. https://doi.org/10.1139/x05-234
Curtu AL (2006) Patterns of genetic variation and hybridization in a mixed oak (Quercus spp.) forest. Cuvillier, Göttingen
de la Torre AR, Roberts DR, Aitken SN (2014) Genome-wide admixture and ecological niche modelling reveal the maintenance of species boundaries despite long history of interspecific gene flow. Molec Ecol 23:2046–2059. https://doi.org/10.1111/mec.12710
Development Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molec Ecol Res 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Futuyma DJ (2005) Evolution. Sinauer, Sunderland
González-Rodríguez A, Arias DM, Valencia S, Oyama K (2004) Morphological and RAPD analysis of hybridization between Quercus affinis and Quercus laurina (Fagaceae), two Mexican red oaks. Amer J Bot 91:401–409. https://doi.org/10.3732/ajb.91.3.401
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, Zapopan
Grant V (1981) Plant speciation. Columbia University Press, New York
Guichoux E, Garnier-Géré P, Lagache L, Lang T, Boury C, Petit RJ (2013) Outlier loci highlight the direction of introgression in oaks. Molec Ecol 22:450–462. https://doi.org/10.1111/mec.12125
Hewitt GM (2002) Hybrid zones. In: Pagel M, Godfray C (eds) Encylopedia of evolution. Oxford University Press, New York, pp 552–556
Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920. https://doi.org/10.1093/molbev/msp296
Howard DJ, Preszler R, Williams J, Fenchel S, Boecklen WJ (1997) How discrete are oak species? insights from a hybrid zone between Quercus grisea and Quercus gambelii. Evolution 51:747–755. https://doi.org/10.2307/2411151
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
Kampfer S, Lexer C, Glössl J, Steinkellner H (1998) Characterization of (GA)n microsatellite loci from Quercus robur. Hereditas 129:183–186. https://doi.org/10.1111/j.1601-5223.1998.00183.x
Kremer A, LeCorre V (2012) Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity 108:375–385. https://doi.org/10.1038/hdy.2011.81
Lefort F, Douglas GC (1999) An efficient micro-method of DNA isolation from mature leaves of four hardwood tree species Acer, Fraxinus, Prunus and Quercus. Ann Forest Sci 56:259–263. https://doi.org/10.1051/forest:19990308
McVaugh R (1974) Flora Novo-Galiciana. University of Michigan, Michigan
Moran EV, John Willis, Clark JS (2012) Genetic evidence for hybridization in red oaks (Quercus sect. Lobatae, Fagaceae). Amer J Bot 99:92–100. https://doi.org/10.3732/ajb.1100023
Morán P, Marco-Rius F, Megías M, Covelo-Soto L, Pérez-Figueroa A (2013) Environmental induced methylation changes associated with seawater adaptation in brown trout. Aquaculture 92–395:77–83. https://doi.org/10.1016/j.aquaculture.2013.02.006
Muir G, Schlötterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Molec Ecol 14:549–561. https://doi.org/10.1111/j.1365-294X.2004.02418.x
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 9:507–522
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
Oksanen J, Kindt R, Legendre P et al (2009) Vegan: community ecology package. Available at https://cran.r-project.org, https://github.com/vegandevs/vegan
Peñaloza-Ramírez JM, González-Rodríguez A, Mendoza-Cuenca L, Caron H, Kremer A, Oyama K (2010) Interespecific gene flow in a multispecies oak hybrid zone in the Sierra Tarahumara of Mexico. Ann Bot (Oxford) 105:389–399. https://doi.org/10.1093/aob/mcp301
Petit RJ (2004) Biological invasions at the gene level. Diversity Distrib 10:159–165. https://doi.org/10.1111/j.1366-9516.2004.00084.x
Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164. https://doi.org/10.1046/j.1469-8137.2003.00944.x
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 655–662
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotypes data. Genetics 155:945–959
Rajora O, Dancik B (2000) Population genetic variation, structure, and evolution in Engelmann spruce, white spruce, and their natural hybrid complex in Alberta. Canad J Bot 78:768–780. https://doi.org/10.1139/b00-054
Rieseberg LH, Wood TE, Baack EJ (2006) The nature of plant species. Nature 440:524–527. https://doi.org/10.1038/nature04402
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 227–236
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 Brook
Rushton BS (1993) Natural hybridization within the genus Quercus L. Ann Sci Forest 50:73–90. https://doi.org/10.1051/forest:19930707
Rzedowski J (1978) Vegetación de México. Limusa, México
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
Savolainen O, Lascoux M, Merilä J (2013) Ecological genomics of local adaptation. Nat Rev Genet 14:807–820. https://doi.org/10.1038/nrg3522
Steinkellner H, Fluch S, Turetschek E et al (1997) Identification and characterization of (GA/CT)n—microsatellite loci from Quercus petraea. Pl Molec Biol 33:1093–1096. https://doi.org/10.1023/A:1005736722794
Stockwell DRB, Noble IR (1992) Introduction of sets of rules from animal distribution data: a robust and informative method of analysis. Math Comput Simul 33:385–390. https://doi.org/10.1016/0378-4754(92)90126-2
Stockwell DRB, Peters DP (1999) The GARP modelling system: problems and solutions to automated spatial prediction. Int J Geogr Inf Syst 13:143–158. https://doi.org/10.1080/136588199241391
Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504. https://doi.org/10.1093/bioinformatics/btn478
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. https://doi.org/10.3732/ajb.91.9.1352
Trelease W (1924) The American oaks. Natl Acad Sci 20:1–255
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 México
Valencia S (2004) Diversidad del género Quercus en México. Bol Soc Bot Méx 75:33–53. https://doi.org/10.17129/botsci.1692
Van Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molec Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Van Valen L (1976) Ecological species, multispecies and oaks. Taxon 25: 233–239. http://www.jstor.org/stable/1219444
Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883. https://doi.org/10.1111/j.1558-5646.2008.00482.x
Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Nat Acad Sci USA 88:2540–2544. https://doi.org/10.1073/pnas.88.6.2540
Wood ET, Nakazato T (2009) Investigating species boundaries in the Giliopsis group of Ipomopsis (Polemoniaceae): strong discordance among molecular and morphological markers. Amer J Bot 96:853–861. https://doi.org/10.3732/ajb.0800153
Wu C-I (2001) The genic view of the process of speciation. J Evol Biol 14:851–865. https://doi.org/10.1046/j.1420-9101.2001.00335.x
Wu C-I, Ting C-T (2004) Genes and speciation. Nat Rev Genet 5:114–122. https://doi.org/10.1038/nrg1269
Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists: a Primer. Elsevier, New York
Acknowledgements
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.
Funding
This work was supported by the graduate programme Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM) and by CONACyT doctoral scholarship [188873] 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 [240136] to KO, and by CONACyT-ECOS NORD [grant M03-A01] to AK and KO.
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Online Resource 1. Sampled populations, taxonomical assignment of Quercus magnoliifolia (Qm) and Q. resinosa (Qr), leaf shape morphological assignment using geometric morphometric by individuals per population, elevation, latitude and longitude.
Online Resource 2. Distribution of Quercus magnoliifolia, Q. resinosa and intermediates individuals identified using leaf shape analysis along the biogeographical regions in Mexico.
Online Resource 3. Chi-squared results (χ2) of omission and commission values obtained with real records and random records across the 10 independent repetition models of GARP and MAXENT obtained for Quercus magnoliifolia and Q. resinosa.
Online Resource 4. Principal component analysis scores of climate variables (PCA-Env. 1 and PCA-Env. 2) analysed to determine the niche overlap and niche divergence between Quercus magnoliifolia and Q. resinosa obtained with ecospat.
Online Resource 5. Genetic assignment by leaf shape morphological assignment of Quercus magnoliifolia, Q. resinosa and intermediates individuals along biogeographical province of Central Plateau, Sierra Madre Occidental, Sierra Madre del Sur and Trans-Mexican Volcanic Belt the main area of sympatry.
Online Resource 6. Genetic assignment of Quercus magnoliifolia, Q. resinosa and intermediates individuals using the admixture proportion for K = 2, obtained with STRUCTURE.
Online Resource 7. Digital image of a leaf of Quercus magnoliifolia and Q. resinosa showing the fan with the 80 radial guidelines and the 29 semilandmarks.
Online Resource 8. a, b Plots of niche overlap densities between the environmental ranges of Quercus magnolifolia and Q. resinosa. c The available environment in the study areas; green and red lines indicate the comparison of the two species at the same time from the sympatric with populations with the same background area. d The correlation circle shows the loadings of individual environmental variables to the two PCA axes and the contribution of each variable to the construction of the PCA-Env.
Online Resource 9. Maximum probability to the most probable genetic group for Quercus magnoliifolia and Q. resinosa.
Online Resource 10. Structure plot for Quercus magnoliifolia and Q. resinosa for the genetic proportion K = 6 genetic groups.
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Albarrán-Lara, A.L., Petit, R.J., Kremer, A. et al. Low genetic differentiation between two morphologically and ecologically distinct giant-leaved Mexican oaks. Plant Syst Evol 305, 89–101 (2019). https://doi.org/10.1007/s00606-018-1554-8
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DOI: https://doi.org/10.1007/s00606-018-1554-8