Abstract
In this study, the effect of hybridization on the interspecific differentiation of two species of red oaks, Quercus acutifolia and Q. grahamii, was evaluated. It is thought that hybridization is possible between these two species since they can inhabit adjacently and have periods of synchronous flowering. In addition, individuals with intermediate morphological attributes have been detected within their populations. To resolve this question, samples were collected from 280 adult individuals from 28 sampling locations: 17 of Q. acutifolia and 11 of Q. grahamii. To identify the individuals belonging to the parental species and those with the presence of hybridization, the individuals were genotyped with 10 nuclear microsatellite loci. To determine the patterns of leaf variation, two sets of morphological traits were considered: the first was 22 foliar morphological measurements, and the second was a geometric morphometry analysis using 40 two-dimensional pseudolandmarks. The results of the analysis of genetic allocation revealed that a large proportion of individuals from all populations showed evidence of introgression in their genomes. The morphological comparison showed that there was a clear differentiation between individuals classified as purebred members of the species Q. acutifolia and Q. grahamii. Individuals with evidence of primary hybridization (F1) were scarce and had morphologies similar to those of the Q. grahamii species. On the other hand, introgressed individuals (F2) seemed to be very similar to their genetically closest parents. The results show that the patterns of foliar morphological variation are not very useful for detecting hybridization events between species with continuous genetic exchange.
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References
Abbott RJ (2017) Plant speciation across environmental gradients and the occurrence and nature of hybrid zones. J Syst Evol 55:238–258. https://doi.org/10.1111/jse.12267
Albarrán-Lara AL, Mendoza-Cuenca L, Valencia-Ávalos 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
Alberto FJ, Aitken SN, Alía R, González-Martínez SC, Hänninen H, Kremer A, Savolainen O (2013) Potential for evolutionary responses to climate change - evidence from tree populations. Global Change Biol 19:1645–1661. https://doi.org/10.1111/gcb.12181
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.1471-8286.2002.00282.x
An M, Deng M, Zheng SS, Jiang XL, Song YG (2017) Introgression threatens the genetic diversity of Quercus austrocochinchinensis (Fagaceae), an endangered oak: A case inferred by molecular markers. Frontiers Pl Sci 8:1–15. https://doi.org/10.3389/fpls.2017.00229
Arnold ML, Bulger MR, Burke JM, Hempel AL, Williams JH (1999) Natural hybridization: how low can you go and still be important? Ecology 80:371. https://doi.org/10.2307/176618
Bodenes C, Joandet S, Laigret F, Kremer A (1997) Detection of genomic regions differentiating two closely related oak species Quercus petraea (Matt.) Liebl. and Quercus robur L. Heredity 78:433–444
Brock CD, Wagner CE (2018) The smelly path to sympatric speciation? Molec Ecol 27:4153–4156. https://doi.org/10.1111/mec.14845
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.1999.1046
Cannon CH, Lerdau MT (2019) Demography and destiny: The syngameon in hyperdiverse systems. Proc Natl Acad Sci USA 116:8105–8105. https://doi.org/10.1073/pnas.1902040116
Cannon CH, Petit RJ (2019) The oak syngameon: more than the sum of its parts. New Phytol 226:978–983. https://doi.org/10.1111/nph.16091
Cavender-Bares J, González-Rodríguez A, Eaton DAR, Hipp AAL, Beulke A, Manos PS (2015) Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): a genomic and population genetics approach. Molec Ecol 24:3668–3687. https://doi.org/10.1111/mec.13269
Cavender-Bares J (2019) Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution. New Phytol 221:669–692. https://doi.org/10.1111/nph.15450
Chatterji S, Pachter L (2006) Reference based annotation with GeneMapper. Genome Biol 7:R29. https://doi.org/10.1186/gb-2006-7-4-r29
Chen JJ (2010) The Hardy-Weinberg principle and its applications in modern population genetics. Frontiers Biol 5:348–353. https://doi.org/10.1007/s11515-010-0580-x
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. doi: https://doi.org/10.1186/1471-2148-7-218
Durand E, Jay F, Gaggiotti O, François O (2009) Spatial inference of admixture proportions and secondary contact zones. Molec Biol Evol 26:1963–1973. https://doi.org/10.1093/molbev/msp106
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, Laval G, Schneider S (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50. https://doi.org/10.1177/117693430500100003
Friedrich S, Konietschke F, Pauly M (2018) Analysis of Multivariate Data and Repeated Measures Designs with the R Package MANOVA.RM. Available at: http://arxiv.org/abs/1801.08002
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. https://doi.org/10.3732/ajb.91.3.401
González-Rodríguez A, Oyama K (2005) Leaf morphometric variation in Quercus affinis and Q. laurina (Fagaceae), two hybridizing Mexican red oaks. Bot J Linn Soc 147:427–435. https://doi.org/10.1111/j.1095-8339.2004.00394.x
Grime JP (2006) Trait convergence and trait divergence in herbaceous plant communities: Mechanisms and consequences. J Veg Sci 17:255–260. https://doi.org/10.1111/j.1654-1103.2006.tb02444.x
Gugger P, Ikegami M, Sork VL (2013) Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata Née. Molec Ecol 22:3598–3612. https://doi.org/10.1111/mec.12317
Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372 https://www.jstor.org/stable/2532296
Hipp AL (2015) Should hybridization make us skeptical of the oak phylogeny? Int Oaks 26:9–18
Hipp AL, Manos PS, González-Rodríguez A, Hahn M, Kaproth M, McVay JD, Cavender-Bares J (2018) Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity. New Phytol 217:439–452. https://doi.org/10.1111/nph.14773
Hochkirch A (2013) Hybridization and the origin of species. J Evol Biol 26:247–251. https://doi.org/10.1111/j.1420-9101.2012.02623.x
Johnen L, de Souza TB, Rocha DM, Parteka LM, González-Elizondo MS, Trevisan R, Chaluvadi SR, Bennetzen JL, Vanzela AL (2020) Allopolyploidy and genomic differentiation in holocentric species of the Eleocharis montana complex (Cyperaceae). Pl Syst Evol 306:1–17. https://doi.org/10.1007/s00606-020-01666-8
Kampfer S, Lexer C, Glössl J, Steinkellner H (1998) Characterization of (GA)n microsatellite 718 loci from Quercus robur. Hereditas 129:183–186
Klein EK, Lagache-Navarro L, Petit RJ (2017) Demographic and spatial determinants of hybridization rate. J Ecol 105:29–38. https://doi.org/10.1111/1365-2745.12674
Korkmaz S, Goksuluk D, Zararsiz G (2019) MVN: An R Package for Assessing Multivariate Normality. Available at: http://www.biosoft.hacettepe.edu.tr/MVN/
Kremer A, Dupouey JL, Deans JD, Cottrell J, Csaikl U, Finkeldey R, Ducousso A (2002) Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Ann Forest Sci 59:777–787. https://doi.org/10.1051/forest:2002065
Kremer A, Abbott AG, Carlson JE, Manos PS, Plomion C, Sisco P, Staton ME, Ueno S, Vendramin GG (2012) Genomics of Fagaceae Tree Genet Genomes 8:583–610. https://doi.org/10.1007/s11295-012-0498-3
Kusak J, Fabbri E, Galov A, Gomerčić T, Arbanasić H, Caniglia R, Galaverni M, Reljić S, Huber D, Randi E (2018) Wolf-dog hybridization in Croatia. Veterin Arh 88:375–395. https://doi.org/10.24099/vet.arhiv.170314
López-Caamal A, del Carmen R-A, Zepeda-Rodríguez A, Mussali-Galante P, Tovar-Sánchez E (2017) Micromorphological character expression of the hybrid Quercus × dysophylla and its parental species (Q. crassifolia and Q. crassipes). Bot Sci 95:375–389. https://doi.org/10.17129/botsci.875
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237. https://doi.org/10.1016/j.tree.2005.02.010
Martínez-Cabrera D, Zavala-Chávez F, Terrazas T (2011) Estudio morfométrico de Quercus sartorii y Q. xalapensis (Fagaceae). Rev Mex Biodivers 82:551–568
McCauley R, Cortés-Palomec A, Oyama K (2019) Species diversification in a lineage of Mexican red oaks (Quercus section Lobatae subsection Racemiflorae)—the interplay between distance, habitat, and hybridization. Tree Genet Genomes 15:27. https://doi.org/10.1007/s11295-019-1333-x
Murrell P (2005) R Graphics. Chapman & Hall/CRC Press, Boca Raton, New York, London. Available at: https://www.stat.auckland.ac.nz/~paul/RGraphics/rgraphics.html
Nielsen E, Bach L, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Molec Ecol Notes 6:971–973
Nixon K (1993) The genus Quercus in Mexico. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of México: origins and distribution. Oxford University Press, New York, pp 447–458
Ogaya R, Peñuelas J (2007) Leaf mass per area ratio in Quercus ilex leaves under a wide range of climatic conditions. The importance of low temperatures. Acta Oecol 31:168–173. https://doi.org/10.1016/j.actao.2006.07.004
Oyama K, Herrera-Arroyo ML, Rocha-Ramírez V, Benítez-Malvido J, Ruiz-Sánchez E, González-Rodríguez, (2017) Gene flow interruption in a recently human-modified landscape: The value of isolated trees for the maintenance of genetic diversity in a Mexican endemic red oak. Forest Ecol Managem 390:27–35. https://doi.org/10.1016/j.foreco.2017.01.018
Oyama K, Ramírez-Toro W, Peñaloza-Ramírez JM, Pérez-Pedraza AE, Torres-Miranda CA, Ruiz-Sánchez E, González-Rodríguez A (2018) High genetic diversity and connectivity among populations of Quercus candicans, Quercus crassifolia, and Quercus castanea in a heterogeneous landscape in Mexico. Trop Conserv Sci 11:1–14. https://doi.org/10.1177/1940082918766195
Pardo A, Ruiz MA (2002) SPSS 11: Guía para el análisis de datos. Mc Graw Hill, Madrid. Available at: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=camoa.xis&method=post&formato=2&cantidad=1&expresion=mfn=001582
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. https://doi.org/10.1093/aob/mcp301
Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24:386–393. https://doi.org/10.1016/j.tree.2009.02.011
Pollock LJ, Bayly MJ, Vesk PA (2015) The roles of ecological and evolutionary processes in plant community assembly: The environment, hybridization, and introgression influence co-occurrence of Eucalyptus. Amer Naturalist 185:784–796. https://doi.org/10.1086/680983
Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rodríguez-Rivera IS, Romero-Rangel S (2007) Arquitectura foliar de diez especies de encino (Quercus, Fagaceae) de México. Acta Bot Mex 81:9–34. https://doi.org/10.21829/abm81.2007.1049
Rodríguez-Gómez F, Oyama K, Ochoa-Orozco M, Mendoza-Cuenca L, Gaytán-Legaria R, González-Rodríguez A (2018) Phylogeography and climate-associated morphological variation in the endemic white oak Quercus deserticola (Fagaceae) along the Trans-Mexican Volcanic Belt. Botany 96:121–133. https://doi.org/10.1139/cjb-2017-0116
Rohlf FJ, Slice D (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Biol 39:40–59. https://doi.org/10.2307/2992207
Rohlf FJ (2005) tpsDig, digitize landmarks and outlines, version 2.05. In: Department of Ecology and Evolution. State University of New York at Stony Brook, New York
Romero Rangel S (2006) Revisión taxonómica del complejo Acutifoliae (Fagaceae) con énfasis en su representación en México. Acta Bot Mex 76:1–45. https://doi.org/10.21829/abm76.2006.106
Romero S, Lira R, Dávila P (2000) A phenetic study of the taxonomic delimitation of Quercus acutifolia and Q. conspersa (Fagaceae). Brittonia 52:177–187. https://doi.org/10.2307/2666509
Rosas T, Mencuccini M, Barba J et al (2019) Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient. New Phytol 223:632–646. https://doi.org/10.1111/nph.15684
Santos-Fernandez E (2014) Johnson: Johnson Transformation. R package version 1.4. Avaliable at: https://CRAN.R-project.org/package=Johnson, Accessed 12 March 2020
Sheets HD (2007) Integrated Morphometrics Package (IMP) 6, 2007. Available at: https://www.animal-behaviour.de/imp/. Accessed 1 Apr 2020
Soltis PS (2013) Hybridization, speciation and novelty. J Evol Biol 26:291–293. https://doi.org/10.1111/jeb.12095
Sork VL, Riordan E, Gugger PF, Fitz-Gibbon S, Wei X, Ortego J (2016) Phylogeny and introgression of California scrub white oaks (Quercus section Quercus). Int Oaks 27:61–74
Steinkellner H, Fluch S, Turetschek E, Lexer C, Streiff R, Kremer A, Glössl J (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
Sullivan AR, Owusu SA, Weber JA et al (2016) Hybridization and divergence in multi-species oak (Quercus) communities. Bot J Linn Soc 181:99–114. https://doi.org/10.1111/boj.12393
Team RC (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: https://www.R-project.org/
Toro-Ibacache MV, Manriquez-Soto G, Suazo-Galdames I (2010) Morfometría geométrica y el estudio de las formas biológicas: de la morfología descriptiva a la morfología cuantitativa. Int J Morphol 28:977–990. https://doi.org/10.4067/S0717-95022010000400001
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 (1929) American oaks. Mem Natl Acad Sci 20:1–255
Valencia-Ávalos S (2004) Diversidad del género Quercus (Fagaceae) en México. Bot Sci 75:33–53. https://doi.org/10.17129/botsci.1692
Valencia-Ávalos S, Flores-Franco G, Jiménez-Ramírez J (2015) Article A nomenclatural revision of Quercus acutifolia, Q. conspersa and Q. grahamii (Lobatae, Fagaceae). Phytotaxa 218:289–294. https://doi.org/10.11646/phytotaxa.218.3.7
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. https://doi.org/10.1007/s11295-014-0710-8
Valencia-Cuevas L, Musali-Galante P, Piñero D, Castillo-Mendoza E, Rangel-Altamirano G, Tovar-Sánchez E (2015) Hybridization of Quercus castanea (Fagaceae) across a red oak species gradient in Mexico. Plant Syst Evol 301:1085–1097. https://doi.org/10.1007/s00606-014-1151-4
Van Oosterhout C, 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
Viscosi V, Fortini P, Slice DE, Loy A, Blasi C (2009a) Geometric morphometric analyses of leaf variation in four oak species of the subgenus Quercus (Fagaceae). Pl Biosyst 143:575–587. https://doi.org/10.1080/11263500902775277
Viscosi V, Lepais O, Gerber S, Fortini P (2009b) Leaf morphological analyses in four European oak species (Quercus) and their hybrids: A comparison of traditional and geometric morphometric methods. Pl Biosyst 143:564–574. https://doi.org/10.1080/11263500902723129
Whitney KD, Ahern JR, Campbell LG, Albert LP, King MS (2010) Patterns of hybridization in plants. Perspect Pl Ecol Evol Syst 12:175–182. https://doi.org/10.1016/j.ppees.2010.02.002
Wickham H (2016) Ggplot2: Elegant graphics for data analysis, 2nd edn. Springer, Cham, pp 3–253. https://doi.org/10.1007/978-3-319-24277-4
Zar J (1999) Bioestatistical analysis, 2nd edn. Prentice Hall, Englewood Cliffs, New Jersey
Zeng YF, Liao WJ, Petit RJ, Zhang DY (2011) Geographic variation in the structure of oak hybrid zones provides insights into the dynamics of speciation. Molec Ecol 20:4995–5011. https://doi.org/10.1111/j.1365-294X.2011.05354.x
Acknowledgements
We thank R. Aguilar-Romero, C.D. Ortega Martínez, F. Hernández Najarro, F.S. Maradiaga Ceceña and J. Llanderal Mendoza for field and laboratory support. This paper constitutes a product of the Graduate Program Posgrado en Ciencias Biológicas, UNAM of AP-P.
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This study was supported by the Consejo Nacional de Ciencia y Tecnología (México) grant 422776 to AP-P, and the Dirección General de Asuntos del Personal Académico, Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica at Universidad Nacional Autónoma de México, grants IV 201016 to KO and IA208218 to AT-M.
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Online Resource 1. The null allele detection analysis.
Online Resource 2. Leaf digitized images with the position of 40 landmarks for the geometric morphometric analysis.
Online Resource 3. Shapiro–Wilk test for all morphological traits by genetic group.
Online Resource 4. Wilk's lambda analysis and ANOVA for all the morphological traits by genetic group.
Online Resource 5. Principal component analysis for the 22 morphological traits.
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Pérez-Pedraza, A., Rodríguez-Correa, H., Valencia-Ávalos, S. et al. Effect of hybridization on the morphological differentiation of the red oaks Quercus acutifolia and Quercus grahamii (Fagaceae). Plant Syst Evol 307, 37 (2021). https://doi.org/10.1007/s00606-021-01757-0
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DOI: https://doi.org/10.1007/s00606-021-01757-0