Abstract
Sympatric hybridizing oak species provide a model system for studying local adaptation. Disjunct populations of Quercus rubra L. and Quercus ellipsoidalis E. J. Hill at the northern edge of their distribution may harbor important reservoirs of adaptive genetic variation. Genic (expressed sequence tag- simple sequence repeat = EST-SSR) and non-genic nuclear microsatellite (nuclear SSR = nSSR) markers were used to estimate neutral and potentially adaptive genetic variation in these two supposedly interfertile oak species showing different adaptations to drought. Eleven populations of putative Q. rubra and Q. ellipsoidalis located in the Western Upper Peninsula of Michigan were characterized using seven EST-SSRs and eight nSSRs. Bayesian cluster analysis revealed two distinct groups corresponding to each species with evidence of low levels of potential introgression. A comparison of the genetic structure of adult trees and seedlings revealed no evidence for selection against hybrids. Overall, similar levels of genetic variation and differentiation between populations and species were found at both EST-SSRs and nSSRs indicating that most EST-SSRs chosen reflect neutral variation. Two loci, 3A05 (nSSR) and GOT021 (EST-SSR, putative histidine kinase 4-like), were identified as putative outlier loci between species showing largely reduced variation in Q. ellipsoidalis. Future analyses of an increased number of EST-SSRs located in functional genes will allow the identification of genes involved in the reproductive isolation between both species.
Similar content being viewed by others
References
Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America. Tree Physiol 7:227–238
Aldrich PR, Cavender-Bares J (2011) Quercus wild crop relatives: genomic and breeding resources. In: Kole C (ed). 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
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Antao T, Lopes A, Lopes R, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a F ST -outlier method. BMC Bioinforma 9:323
Arnold ML, Martin NH (2010) Hybrid fitness across time and habitats. Trends Ecol Evol 25:530–536
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 BVW, Warren Herbert Jr. (2004) Michigan trees, revised and updated: a guide to the trees of the Great Lakes region. University of Michigan Press, Ann Arbor
Beaumont MA (2005) Adaptation and speciation: what can F ST tell us? Trends Ecol Evol 20:435–440
Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. P Roy Soc B-Biol Sci 263:1619–1626
Boavida LC, Silva JP, Feijo JA (2001) Sexual reproduction in the cork oak (Quercus suber L). II. Crossing intra- and interspecific barriers. Sex Plant Reprod 14:143–152
Burger WC (1975) The species concept in Quercus. Taxon 24:45–50
Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. Heredity 99:616–623
Cavender-Bares J, Pahlich A (2009) Molecular, morphological, and ecological niche differentiation of sympatric sister oak species, Quercus virginiana and Q. geminata (Fagaceae). Am J Bot 96:1690–1702
Chesnoiu EN, Sofletea N, Curtu AL, Toader A, Radu R, Enescu M (2009) Bud burst and flowering phenology in a mixed oak forest from Eastern Romania. Ann For Res 52:199–206
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676
Coyer JA, Hoarau G, Pearson G, Mota C, Juterbock A, Alpermann T, John U, Olsen JL (2011) Genomic scans detect signatures of selection along a salinity gradient in populations of the intertidal seaweed Fucus serratus on a 12 km scale. Mar Genomics 4:41–49
Craft KJ, Ashley MV, Koenig WD (2002) Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central coastal California. Am J Bot 89(11):1792–1798
Curtu A, Gailing O, Finkeldey R (2007a) Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evol Biol 7:218
Curtu A, Gailing O, Leinemann L, Finkeldey R (2007b) Genetic variation and differentiation within a natural community of five oak species (Quercus spp.). Plant Biol 9:116–126
Curtu A, Gailing O, Finkeldey R (2009) Patterns of contemporary hybridization inferred from paternity analysis in a four-oak-species forest. BMC Evol Biol 9:284
Desikan R, Horák J, Chaban C, Mira-Rodado V, Witthöft J, Elgass K, Grefen C, Cheung M-K, Meixner AJ, Hooley R, Neill SJ, Hancock JT, Harter K (2008) The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. PLoS One 3:e2491
Doak DF, Morris WF (2010) Demographic compensation and tipping points in climate-induced range shifts. Nature 467:959–962
Dodd RS, Afzal-Rafii Z (2004) Selection and dispersal in a multispecies oak hybrid zone. Evolution 58:261–269
Dow BD, Ashley MV, Howe HF (1995) Characterization of highly variable (GA/CT) microsatellites in the bur oak, Quercus macrocarpa. Theor Appl Genet 91:137–141
Durand J, Bodenes C, Chancerel E, Frigerio J-M, Vendramin G, 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, Alberto F, Dumoulin P-Y, Guichoux E, de Daruvar A, Kremer A, Plomion C (2010) A fast and cost-effective approach to develop and map EST-SSR markers: oak as a case study. BMC Genomics 11:570
Ellis JR, Burke JM (2007) EST-SSRs as a resource for population genetic analyses. Heredity 99:125–132
Emms SK, Arnold ML (1997) The effect of habitat on parental and hybrid fitness: transplant experiments with Louisiana irises. Evolution 51:1112–1119
ESRI (Environmental Systems Resource Institute) (2009) ArcMap 9.2: ArcGIS for desktop. Redlands, California (http://www.esri.com/software/arcgis/arcgis-for-desktop
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchical structured population. Heredity 103:285–298
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578
Gailing O, Lind J, Lilleskov E (2012) 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
Goicoechea PG, Petit RJ, Kremer A (2012) Detecting the footprints of divergent selection in oaks with linked markers. Heredity. doi:10.1038/hdy.2012.51
Hipp AL (2010) Hill’s oak: the taxonomy and dynamics of a Western Great Lake endemic. Arnoldia 67:1–13
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
Howard DJ, Preszler RW, 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
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
Jimenez P, Agundez D, Alia R, Gil L (1999) Genetic variation in central and marginal populations of Quercus suber L. Silvae Genet 48:278–284
Jimenez P, Lopez de Heredia U, Collada C, Lorenzo Z, Gil L (2004) High variability of chloroplast DNA in three Mediterranean evergreen oaks indicates complex evolutionary history. Heredity 93:510–515
Kampfer S, Lexer C, Glössl J, Steinkellner H (1998) Characterization of (GA)n microsatellite loci from Quercus robur. Hereditas 129:183–186
Kremer A, Petit R (1993) Gene diversity in natural populations of oak species. Ann For Sci 50:186s–202s
Kremer A, Dupouey JL, Deans JD, Cottrell J, Csaikl U, Finkeldey R, Espinel S, Jensen J, Kleinschmit J, Van Dam B, Ducousso A, Forrest I, Lopez de Heredia U, Lowe AJ, Tutkova M, Munro RC, Steinhoff S, Badeau V (2002) Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Ann For Sci 59:777–787
Langella O (1999) Populations 1.2.30: a population genetic software CNRS UPR9034
Latter BDH (1973) The island model of population differentiation: a general solution. Genetics 73:147–157
Lepais O, Petit RJ, Guichoux E, Lavabre JE, Alberto F, Kremer A, Gerber S (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242
Lexer C, Kremer A, Petit RJ (2006) Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Mol Ecol 15:2007–2012
Lopez de Heredia U, Valbuena-Carabaña M, Cordoba M, Gil L (2009) Variation components in leaf morphology of recruits of two hybridising oaks [Q. petraea (Matt.) Liebl. and Q. pyrenaica Willd.] at a small spatial scale. Eur J Forest Res 128:543–554
Lorenzo Z, Burgarella C, Lopez de Heredia U, Lumaret R, Petit RJ, Soto A, Gil L (2009) Relevance of genetics for conservation policies: the case of Minorcan cork oaks. Ann Bot-London 104:1069–1076
Luro F, Costantino G, Terol J, Argout X, Allario T, Wincker P, Talon M, Ollitrault P, Morillon R (2008) Transferability of the EST-SSRs developed on Nules clementine (Citrus clementina Hort ex Tan) to other Citrus species and their effectiveness for genetic mapping. BMC Genomics 9:287
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
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 Wildlife Manage 71:1717–1728
Mir C, Toumi L, Jarne P, Sarda V, Di Guisto F, Lumaret R (2006) Endemic North African Quercus afares Pomel originates from hybridisation between two genetically very distant oak species (Q. suber L. and Q. canariensis Willd.): evidence from nuclear and cytoplasmic markers. Heredity 96:175–184
Moran EV, Willis J, Clark JS (2012) Genetic evidence for hybridization in red oaks (Quercus sect. Lobatae, Fagaceae). Am J Bot 99:92–100
Muir G, Fleming CC, Schlötterer C (2001) Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. Mol Biol Evol 18:112–119
Nagy ES, Rice KJ (1997) Local adaptation in two subspecies of an annual plant: implications for migration and gene flow. Evolution 51:1079–1089
Narum SR, Hess JE (2011) Comparison of F ST outlier tests for SNP loci under selection. Mol Ecol Resour 11:184–194
Nei M (1973) Analysis of gene diversity in subdivided populations. P Natl Acad Sci USA 70:3321–3323
Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377
Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Pautasso M (2009) Geographical genetics and the conservation of forest trees. Perspect Plant Ecol 11:157–189
Peakall ROD, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
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 105:389–399
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GenePop (Version-1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rieseberg LH, Ellstrand NC, Arnold M (1993) What can molecular and morphological markers tell us about plant hybridization. CRC Cr Rev Plant Sci 12:213–241
Rosenburg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Rushton B (1993) Natural hybridization within the genus Quercus L. Ann For Sci 50:73s–90s
Salvini D, Bruschi P, Fineschi S, Grossoni P, Kjær ED, Vendramin GG (2009) Natural hybridisation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. within an Italian stand as revealed by microsatellite fingerprinting. Plant Biol 11:758–765
Scotti-Saintagne C, Mariette S, Porth I, Goicoechea PG, Barreneche T, Bodénès C, Burg K, Kremer A (2004) Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. and Q. petraea (Matt.) Liebl.]. Genetics 168:1615–1626
Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. Freeman, San Fransisco
Sork V, Huang S, Wiener E (1993) Macrogeographic and fine-scale genetic structure in a North American oak species, Quercus rubra L. Ann For Sci 50:261s–270s
Steinkellner H, Fluch S, Turetschek E, Lexer C, Streiff R, Kremer A, Burg K, Glossl J (1997) Identification and characterization of (GA/CT)n-microsatellite loci from Quercus petraea. Plant Mol Biol 33:1093–1096
Sullivan AR, Lind JF, McCleary TS, Romero-Severson J, Gailing O (2012) Development and characterization of genomic and gene-based microsatellite markers in North American red oak species. Plant Mol Biol Rep. doi:10.1007/s11105-012-0495-6
Valbuena-Carabaña M, Gonzáles-Martínez SC, Sork VL, Collada C, Soto A, Goicoechea PG, Gil L (2005) Gene flow and hybridisation in a mixed oak forest (Quercus pyrenaica Willd. and Quercus petraea (Matts.) Liebl.) in central Spain. Heredity 95:457–465
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Van Valen L (1976) Ecological species, multispecies, and oaks. Taxon 25:233–239
Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. P Natl Acad Sci 88:2540–2544
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. Forest Ecol Manag 257:1434–1444
Wright S (1922) Coefficients of inbreeding and relationship. Am Nat 56:330–338
Acknowledgments
We would like to thank James Schmierer for his help in sample collection in the Baraga Plains and Dr. Kerry Woods for his help in the identification of populations in the Huron Mountain Wildlife Reserve. Q. rubra and Q. ellipsoidalis reference samples were provided by Jeanne Romero-Severson and Andrew Hipp. Additionally, we would like to thank Jonathan Riehl for invaluable advice and guidance on the construction of many of the graphics. We also thank two anonymous reviewers for their very helpful comments on earlier drafts. Funding for the study came from Michigan Technological University start-up funds 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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. G. Vendramin
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 307 kb)
Rights and permissions
About this article
Cite this article
Lind, J.F., Gailing, O. Genetic structure of Quercus rubra L. and Quercus ellipsoidalis E. J. Hill populations at gene-based EST-SSR and nuclear SSR markers. Tree Genetics & Genomes 9, 707–722 (2013). https://doi.org/10.1007/s11295-012-0586-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-012-0586-4