Leaf morphological and genetic variation between Quercus rubra and Quercus ellipsoidalis: comparison of sympatric and parapatric populations
DOI:
https://doi.org/10.15287/afr.2018.1020Keywords:
traits, EST-SSRs, oaks, hybridizationAbstract
Species boundaries in oaks are often not clear-cut, which is potentially a result of interspecific hybridization with trait introgression and phenotypic plasticity. Quercus rubra L. and Quercus ellipsoidalis E.J. Hill are two interfertile partially sympatric red oak species (section Lobatae) with different adaptations to drought. Quercus ellipsoidalis is the most drought tolerant of the North American red oak species and is characterized by deep tap roots, a shrubby growth and by deeply dissected leaves. Genetic differentiation between species is low for most molecular markers. However, one genic microsatellite in a CONSTANS-like (COL) gene, FIR013, was previously identified as outlier locus under strong divergent selection between species. In this study, we analyzed leaf morphometric traits in neighboring (parapatric) Q. rubra/Q. ellipsoidalis populations and in one sympatric population from the same region along an environmental gradient. Using multivariate statistics of leaf traits both species showed distinct bimodal frequency distributions for the first canonical discriminant function with some overlap in the phenotypic extremes, especially in the sympatric population. Leaf dissection traits showed strong and consistent differentiation between species in sympatric and parapatric populations, while differentiation for leaf size was lower in the sympatric population under more similar environmental conditions. Leaf phenotypes in F1 hybrids and introgressive forms suggested maternal effects and introgression of leaf traits between species. The association of outlier gene copy number at FIR013 with species-discriminating leaf traits in Quercus rubra can be a reflection of population differences since outlier gene copy number and population membership show significant collinearity. Similar environmental selection pressures on outlier alleles and leaf shape could also have resulted in this association. In future studies, segregating full-sib families could be used to test whether outlier alleles and associated genomic regions are indeed associated with leaf traits or other species-discriminating characters.References
Abrams M.D., 1990. Adaptations and responses to drought in Quercus species of North America. Tree Physiology 7:227-238. DOI: 10.1093/treephys/7.1-2-3-4.227 Alberto F.J., Derory J., Boury C., Frigerio J.M., Zimmermann N.E., Kremer A., 2013. Imprints of natural selection along environmental gradients in phenology-related genes of Quercus petraea. Genetics 195:495-512. DOI: 10.1534/genetics.113.153783 Bates D., Machler M., Bolker B.M., Walker S.C., 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1-48. DOI: 10.18637/jss.v067.i01 Bruschi P., Grossoni P., Bussotti F., 2003. Within- and among-tree variation in leaf morphology of Quercus petraea (Matt.) Liebl. natural populations. Trees-Structure and Function 17:164-172. Burns R.M., Honkala B.H., 1990. Silvics of North America, Washington, DC. Chesnoiu E.N., Șofletea N., Curtu A.L., Toader A., Radu R., Enescu M., 2009. Bud burst and flowering phenology in a mixed oak forest from Eastern Romania. Annals of Forest Research 52:199-206. Collins E., Sullivan A.R. Gailing O., 2015. Limited effective gene flow between two interfertile red oak species. Trees-Structure and Function 29:1135-1148. DOI: 10.1007/s00468-015-1194-3 Cottam W.P., Tucker J.M., Santamour Jr. F.S., 1982. Oak hybridization at the University of Utah. State Arboretum of Utah, University of Utah. Curtu A.L., Gailing O., Finkeldey R., 2007. Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evolutionary Biology 7:218. DOI: 10.1186/1471-2148-7-218 Curtu A.L., Gailing O., Finkeldey R., 2009. Patterns of contemporary hybridization inferred from paternity analysis in a four-oak-species forest. BMC Evolutionary Biology 9:284. DOI: 10.1186/1471-2148-9-284 de Heredia U.L., Valbuena-Carabana 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 small spatial scale. European Journal of Forest Research 128:543-554. DOI: 10.1007/s10342-009-0302-6 Fitch R., 2006. WinSTAT for Excel. Fox J., Weisberg S., 2011. An R companion to applied regression. 2nd edition. SAGE Publications, Inc., California. Gailing O., 2008. QTL analysis of leaf morphological characters in a Quercus robur full-sib family (Q. robur x Q. robur ssp. slavonica). Plant Biology 10:624-634. DOI: 10.1111/j.1438-8677.2008.00063.x Gailing O., Bodénès C., Finkeldey R., Kremer A., Plomion C., 2013. Genetic mapping of EST-derived Simple Sequence Repeats (EST-SSRs) to identify QTL for leaf morphological characters in a Quercus robur full-sib family. Tree Genetics & Genomes 9:1361-1367. DOI: 10.1007/s11295-013-0633-9 Gailing O., Lind J., Lilleskov E.A., 2012. Leaf morphological and genetic differentiation between Quercus rubra L. and Q. elliposidalis E. J. Hill populations in contrasting environments. Plant Systematics and Evolution 298:1533-1545. DOI: 10.1007/s00606-012-0656-y Gonzalez-Rodriguez A., Oyama K.E.N., 2005. Leaf morphometric variation in Quercus affinis and Q. laurina (Fagaceae), two hybridizing Mexican red oaks. Botanical Journal of the Linnean Society 147:427-435. DOI: 10.1111/j.1095-8339.2004.00394.x Gugerli F., Walser J.-C., Dounavi K., Holderegger R., Finkeldey R., 2007. Coincidence of small-scale spatial discontinuities in leaf morphology and nuclear microsatellite variation of Quercus petraea and Q. robur in a mixed forest. Annals of Botany 99:713-722. DOI: 10.1093/aob/mcm006 Gurevitch J., Schuepp P.H., 1990. Boundary layer properties of highly dissected leaves: an investigation using an electrochemical fluid tunnel. Plant Cell and Environment 13:783-792. DOI: 10.1111/j.1365-3040.1990.tb01094.x Herrmann D., Barre P., Santoni S., Julier B., 2010. Association of a CONSTANS-LIKE gene to flowering and height in autotetraploid alfalfa. Theoretical and Applied Genetics 121:865-876. DOI: 10.1007/s00122-010-1356-z Hothorn T., Bretz F., Westfall P., 2008. Simultaneous inference in general parametric models. Biometrical Journal 50:346-363. DOI: 10.1002/bimj.200810425 Hsu C.Y., Adams J.P., No K., Liang H.Y., Meilan R., Pechanova O., Barakat A., Carlson J.E., Page G.P., Yuceer C., 2012. Overexpression of Constans homologs CO1 and CO2 fails to alter normal reproductive onset and fall bud set in woody perennial poplar. Plos One 7:e45448. DOI: 10.1371/journal.pone.0045448 IBM. 2015. IBM SPSS Statistics for Windows IBM Corp., Armonk, NY. Jensen R.J., Hokanson S.C., Isebrands J.G., Hancock J.F., 1993. Morphometric variation in oaks of the apostle islands in Wisconsin - evidence of hybridization between Quercus rubra and Q. ellipsoidalis (Fagaceae). American Journal of Botany 80:1358-1366. DOI: 10.1002/j.1537-2197.1993.tb15375.x Khodwekar S., Gailing O., 2017. Evidence for environment-dependent introgression of adaptive genes between two red oak species with different drought adaptations. American Journal of Botany 104:1088-1098. DOI: 10.3732/ajb.1700060 Kleinschmit J.R.G., Bacilieri R., Kremer A., and A. Roloff A., 1995. Comparison of morphological and genetic traits of pedunculate oak (Quercus robur L.) and sessile oak (Q. petraea (Matt.) Liebl.). Silvae Genetica 44:256-269. Kramer P.J., Boyer J.S., 1995. Water relations of plants and soils. Academic Press, San Diego. Kremer A., Dupouey J.L, Deans J.D., Cottrell J., Csaikl U., Finkeldey R., Espinel S., Jensen J., Kleinschmit J., Van Dam B., Ducousso A., Forrest I., Lopez de Heredia U., Lowe A.J., Tutkova M., Munro R.C., Steinhoff S., Badeau V., 2002. Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Annals of Forest Science 59:777-787. DOI: 10.1051/forest:2002065 Lepais O., Petit R.J, Guichoux E., Lavabre J.E., Alberto F., Kremer A., and S. Gerber S., 2009. Species relative abundance and direction of introgression in oaks. Molecular Ecology 18:2228-2242. DOI: 10.1111/j.1365-294X.2009.04137.x Lexer C., Kremer A., Petit R.J., 2006., Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Molecular Ecology 15:2007-2012. DOI: 10.1111/j.1365-294X.2006.02896.x Lind-Riehl J., Gailing O., 2017. Adaptive variation and introgression of a CONSTANS-like gene in North American red oaks. Forests 8:3. DOI: 10.3390/f8010003 Lind-Riehl J.F., Sullivan A.R., Gailing O., 2014. Evidence for selection on a CONSTANS-like gene between two red oak species. Annals of Botany 113:967-975. DOI: 10.1093/aob/mcu019 Lind J., Gailing O., 2013. Genetic structure of Quercus rubra L. and Q. ellipsoidalis E. J. Hill populations at gene-based EST-SSR and nuclear SSR markers. Tree Genetics & Genomes 9:707-722. DOI: 10.1007/s11295-012-0586-4 Mariette S., Cottrell J., Csaikl U.M., Goikoechea P., König A.O., Lowe A.J., Van Dam B.C., Barreneche T., Bodenes C., Streiff R., Burg K., Groppe K., Munro R.C., 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. Moran E. V., Willis J., Clark J.S., 2012. Genetic evidence for hybridization in red oaks (Quercus sect. Lobatae, Fagaceae). American Journal of Botany 99:92-100. DOI: 10.3732/ajb.1100023 Muir G., Schlötterer C., 2005. Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridising oaks (Quercus spp.). Molecular Ecology 14:549-561. DOI: 10.1111/j.1365-294X.2004.02418.x Neophytou C., Dounavi A., Fink S., Aravanopoulos F.A., 2011. Interfertile oaks in an island environment: I. High nuclear genetic differentiation and high degree of chloroplast DNA sharing between Q. alnifolia and Q. coccifera in Cyprus. A multipopulation study. European Journal of Forest Research 130:543-555. DOI: 10.1007/s10342-010-0442-8 Nicotra A.B., Leigh A., Boyce C.K., Jones C.S., Niklas K.J., Royer D.L., Tsukaya H., 2011. The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology 38:535-552. DOI: 10.1071/FP11057 Owusu S. A., Sullivan A.R., Weber J.A., Hipp A.L., Gailing O., 2015. Taxonomic relationships and gene flow in four North American Quercus species. Systematic Botany 40:510-521. DOI: 10.1600/036364415X688754 Petit R.J., Bodénès C., Ducousso A., Roussel G., Kremer A, 2003. Hybridization as a mechanism of invasion in oaks. New Phytologist 161:151-164. DOI: 10.1046/j.1469-8137.2003.00944.x Pritchard J. K., Stephens M., Donnelly P., 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959. Sack L., Holbrook N.M., 2006. Leaf hydraulics. Annual Review of Plant Biology 57:361-381. DOI: 10.1146/annurev.arplant.56.032604.144141 Saintagne C., Bodenes C., Barreneche T., Pot D., Plomion C., Kremer A., 2004. Distribution of genomic regions differentiating oak species assessed by QTL detection. Heredity 92:20-30. DOI: 10.1038/sj.hdy.6800358 Scotti-Saintagne C., Mariette S., Porth I., Goicoechea P.G., Barreneche T., Bodénès C., 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. DOI: 10.1534/genetics.104.026849 Team R., 2015. RStudio: Integrated development for R. RStudio, Inc., Boston, MA. Venables W.N., Ripley B.D., 2002. Modern Applied Statistics with S. 4th edition. Springer, New York. DOI: 10.1007/978-0-387-21706-2 Zhang R., Hipp A.L., Gailing O., 2015. Sharing of chloroplast haplotypes among red oak species suggests interspecific gene flow between neighboring populations. Botany 93:691-700. DOI: 10.1139/cjb-2014-0261
Published
Issue
Section
License
All the papers published in Annals of Forest Research are available under an open access policy (Gratis Gold Open Access Licence), which guaranty the free (of taxes) and unlimited access, for anyone, to entire content of the all published articles. The users are free to “read, copy, distribute, print, search or refers to the full text of these articles”, as long they mention the source.
The other materials (texts, images, graphical elements presented on the Website) are protected by copyright.
The journal exerts a permanent quality check, based on an established protocol for publishing the manuscripts. The potential article to be published are evaluated (peer-review) by members of the Editorial Board or other collaborators with competences on the paper topics. The publishing of manuscript is free of charge, all the costs being supported by Forest Research and Management Institute.
More details about Open Access:
Wikipedia: http://en.wikipedia.org/wiki/Open_access