Abstract
Hybridization is considered to play an important role in speciation and evolution. Given the predicted northward tree migration in the eastern USA due to the impact of climate change, hybridization between related species is expected to become more frequent due to overlapping distribution ranges in the future. Oak species are “hot spots” of contemporary hybridization, serving as model organisms in the development of ecological species concepts. Q. rubra L. and Q. ellipsoidalis E.J. Hill were selected as study species, since they show different ecological requirements but hybridize with each other where both species co-occur. To identify morphological species and differentiation patterns in this species pair in ten populations on the Upper Peninsula of Michigan we investigated both leaf morphological variation, and genetic variation at highly variable microsatellite markers. Cluster analyses using leaf morphological characters revealed two distinct clusters for directly measured leaf characters and three clusters when additionally leaf shape characters were considered. Two populations growing on dry and sandy sites and identified as Q. ellipsoidalis in the field and by genetic assignment analyses were differentiated from the other eight populations at leaf morphological characters. Strong and significant correlations of leaf morphological differences with genetic distances at microsatellite markers but not with geographic distances are consistent with a pattern of isolation by adaptation. Differentiation at genetic and leaf morphological characters between neighboring populations in contrasting environments suggested reproductive isolation between populations of different species, possibly as the result of divergent selection. More extensive sampling along the distribution range of both species and reciprocal transplant experiments between parental environments are necessary to better understand the role of interspecific gene flow and selection in the maintenance of species identity in red oak species (Quercus section Lobatae).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrams MD (1988) Comparative water relationships of 3 successional hard wood species in central Wisconsin. Tree Physiol 4:263–273
Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America. Tree Physiol 7:227–238
Albert DA, Comer PJ (2008) Atlas of early Michigan’s forests, grasslands, and wetlands. Michigan State University Press, East Lansing
Aldrich P, Cavender-Bares J (2011) Quercus. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, forest trees. Springer, Berlin, pp 89–129
Aldrich PR, Michler CH, Sun WL, Romero-Severson J (2002) Microsatellite markers for northern red oak (Fagaceae: Quercus rubra). Mol Ecol Notes 2:472–474
Bacilieri R, Ducousso A, Petit RJ, Kremer A (1996) Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution 50:900–908
Barnes BV, Wagner WH Jr (2004) Michigan Trees, A Guide to the Trees of the Great Lakes Region. The University of Michigan Press, Ann Arbor
Craft KJ, Ashley MV, Koenig WD (2002) Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central coastal California. Amer J Bot 89:1792–1798
Curtu AL, Gailing O, Leinemann L, Finkeldey R (2007) Genetic variation and differentiation within a natural community of five oak species (Quercus spp.). Plant Biol 9:116–126
Curtu AL, Gailing O, Finkeldey R (2009) Patterns of contemporary hybridization inferred from paternity analysis in a four-oak-species forest. BMC Evol Biol 9:284
Dodd RS, Afzal-Rafii Z (2004) Selection and dispersal in a multispecies oak hybrid zone. Evolution 58:261–269
Durand J, Bodenes C, Chancerel E, Frigero J-M, Vendramin GG, Sebastiani F, Buonamici A, Gailing O, Koelewijn H-P, Villani F, Mattioni C, Cherubini M, Goicoechea PG, Herran A, Ikaran Z, Cabane C, Ueno S, de Daruvar A, Kremer A, Plomion C (2010) SSR mining in oak ESTs and bin mapping of 256 loci in a Quercus robur L. full-sib pedigree. BMC Genomics 11:570
Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164–166
Finkeldey R (2000) Genetic variation of oaks (Quercus spp.) in Switzerland. 2. Genetic structures in “pure” and “mixed” forests of pedunculate oak (Q. robur L.) and sessile oak (Q. petraea (Matt.) Liebl.). Silvae Genetica 50:22–30
Fitch R (2006) WinSTAT for Excel
Hipp AL, Weber JA (2008) Taxonomy of Hill’s oak (Quercus ellipsoidalis: Fagaceae): evidence from AFLP data. Syst Bot 33:148–158
Hokanson SC, Isebrands JG, Jensen RJ, Hancock JF (1993) Isozyme variation in oaks of the apostle islands in Wisconsin–genetic structure and levels of inbreeding in Quercus rubra and Q. ellipsoidalis (Fagaceae). Am J Bot 80:1349–1357
Jensen RJ, Hokanson SC, Isebrands JG, Hancock JF (1993) Morphometric variation in oaks of the apostle islands in Wisconsin - evidence of hybridization between Quercus rubra and Q. ellipsoidalis (Fagaceae). Am J Bot 80:1358–1366
Jump AS, Hunt JM, Martinez-Izquierdo JA, Penuelas J (2006) Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Mol Ecol 15:3469–3480
Mariette S, Cottrell J, Csaikl UM, Goikoechea P, König AO, Lowe AJ, Van Dam BC, Barreneche T, Bodenes 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 Genetica 51:72–79
McShea WJ, Healy WM, Devers P, Fearer T, Koch FH, Stauffer D, Waldon J (2007) Forestry matters: Decline of oaks will impact wildlife in hardwood forests. J Wildl Manage 71:1717–1728
Müller-Starck G (1985) Genetic differences between “tolerant” and “sensitive” beeches (Fagus sylvatica L.) in an environmentally stressed adult forest stand. Silvae Genetica 34:241–247
Nixon KC (1997). Quercus. In: Flora of North America Editorial Committee (eds) Flora of North America North of Mexico, vol 3. Oxford University Press, New York, pp 445–447
Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402
Peakall R, Smouse PE (2006) GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Scotti-Saintagne C, Mariette S, Porth I, Goicoechea PG, Barreneche T, Bodenes K, Burg K, Kremer A (2004) Genome scanning of interspecific differentiation between two closely related oak species (Quercus robur L. and Q. petraea (Matt.) Liebl.). Genetics 168:1615–1626
Steinkellner H, Fluch S, Turetschek E, Lexer C, Streiff R, Kremer A, Burg K, Glössl J (1997) Identification and characterization of (GA/CT)n-microsatellite loci from Quercus petraea. Plant Mol Biol 33:1093–1096
Van Valen L (1976) Ecological species, multispecies and oaks. Taxon 25:233–239
Voss EG (1985) Michigan Flora, Part II. University of Michigan Herbarium, Ann Arbor
Woodall CW, Oswalt CM, Westfall JA, Perry CH, Nelson MD, Finley AO (2009) An indicator of tree migration in forests of the eastern United States. For Ecol Manage 257:1434–1444
Acknowledgments
We would like to thank James Schmierer for his help in identifying stands in the Baraga Plains and in sample collection, and Dr. Kerry Woods for his help in the identification of Q. rubra populations in the Huron Mountain Wildlife Reserve. For their help in preparing and measuring the leaves we would like to thank Erin Hickey and Joanna Rogers. Funding for the study came from start-up funds of Michigan Technological University to Oliver Gailing, the Michigan Technological University Research Excellence fund, the USDA McIntire Stennis fund, the Huron Mountain Wildlife Foundation, the Hanes Trust, and the NSF Plant Genome Research program (NSF 1025974). We like to thank two anonymous reviewers for their helpful comments.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
606_2012_656_MOESM1_ESM.ppt
Supplementary Fig. 1: Scatter plot of factor 1 and factor 2 of PCA1. Samples from Q. ellipsoidalis populations FC-C and FC-E cluster together (see lower left side) (PPT 227 kb)
Rights and permissions
About this article
Cite this article
Gailing, O., Lind, J. & Lilleskov, E. Leaf morphological and genetic differentiation between Quercus rubra L. and Q. ellipsoidalis E.J. Hill populations in contrasting environments. Plant Syst Evol 298, 1533–1545 (2012). https://doi.org/10.1007/s00606-012-0656-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-012-0656-y