Forest trees generally show high levels of local adaptation and efforts focusing on understanding adaptation to climate will be crucial for species survival and management. Here, we address fundamental questions regarding the molecular basis of adaptation in undomesticated forest tree populations to past climatic environments by employing an integrative quantitative genetics and landscape genomics approach. Using this comprehensive approach, we studied the molecular basis of climate adaptation in 433 Populus trichocarpa (black cottonwood) genotypes originating across western North America. Variation in 74 field-assessed traits (growth, ecophysiology, phenology, leaf stomata, wood, and disease resistance) was investigated for signatures of selection (comparing QST-FST) using clustering of individuals by climate of origin (temperature and precipitation). 29,354 SNPs were investigated employing three different outlier detection methods and marker-inferred relatedness was estimated to obtain the narrow-sense estimate of population differentiation in wild populations. In addition, we compared our results with previously assessed selection of candidate SNPs using the 25 topographical units (drainages) across the P. trichocarpa sampling range as population groupings. Narrow-sense QST for 53% of distinct field traits was significantly divergent from expectations of neutrality (indicating adaptive trait variation); 2,855 SNPs showed signals of diversifying selection and of these, 118 SNPs (within 81 genes) were associated with adaptive traits (based on significant QST). Many SNPs were putatively pleiotropic for functionally uncorrelated adaptive traits, such as autumn phenology, height, and disease resistance. Evolutionary quantitative genomics in P. trichocarpa provides an enhanced understanding regarding the molecular basis of climate-driven selection in forest trees and we highlight that important loci underlying adaptive trait variation also show relationship to climate of origin. We consider our approach the most comprehensive, as it uncovers the molecular mechanisms of adaptation using multiple methods and tests. We also provide a detailed outline of the required analyses for studying adaptation to the environment in a population genomics context to better understand the species' potential adaptive capacity to future climatic scenarios.

Corn Soybean and Wheat Quality Research Unit United States Department of Agriculture Wooster Ohio 44691 United States of America

Département des Sciences du Bois et de la Forêt Faculté de Foresterie de Géographie et de Géomatique Université Laval Québec QC G1V 0A6 Canada

Department of Biology and Centre for Forest Biology University of Victoria Victoria BC V8W 3N5 Canada

Department of Botany University of British Columbia Vancouver BC V6T 1Z4 Canada

Department of Ecology and Environmental Science Umeå University Umeå SE 901 87 Sweden

Department of Forest and Conservation Sciences University of British Columbia Vancouver BC V6T 1Z4 Canada

Department of Genetics and Physiology of Forest Trees Czech University of Life Sciences Prague 165 21 Czech Republic

Department of Wood Science University of British Columbia Vancouver BC V6T 1Z4 Canada

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Savolainen O, Lascoux M, Merila J. Ecological genomics of local adaptation. Nature Review Genetics. 2013;14(11):807–20. PubMed

Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications. 2008;1(1):95–111. 10.1111/j.1752-4571.2007.00013.x PubMed DOI PMC

Allendorf FW, Hohenlohe PA, Luikart G. Genomics and the future of conservation genetics. Nature Reviews Genetics. 2010;11(10):697–709. 10.1038/nrg2844 PubMed DOI

Eckert AJ, Bower AD, Gonzalez-Martinez SC, Wegrzyn JL, Coop G, Neale DB. Back to nature: ecological genomics of loblolly pine (Pinus taeda, Pinaceae). Molecular Ecology. 2010;19(17):3789–805. 10.1111/j.1365-294X.2010.04698.x PubMed DOI

Tsumura Y, Uchiyama K, Moriguchi Y, Ueno S, Ihara-Ujino T. Genome scanning for detecting adaptive genes along environmental gradients in the Japanese conifer, Cryptomeria japonica. Heredity. 2012;109(6):349–60. 10.1038/hdy.2012.50 PubMed DOI PMC

Chen J, Kallman T, Ma X, Gyllenstrand N, Zaina G, Morgante M, et al. Disentangling the Roles of History and Local Selection in Shaping Clinal Variation of Allele Frequencies and Gene Expression in Norway Spruce (Picea abies). Genetics. 2012;191(3):865–81. 10.1534/genetics.112.140749 PubMed DOI PMC

Keller SR, Levsen N, Olson MS, Tiffin P. Local Adaptation in the Flowering-Time Gene Network of Balsam Poplar, Populus balsamifera L. Molecular Biology and Evolution. 2012;29(10):3143–52. PubMed

Holliday JA, Ralph SG, White R, Bohlmann J, Aitken SN. Global monitoring of autumn gene expression within and among phenotypically divergent populations of Sitka spruce (Picea sitchensis). New Phytologist. 2008;178(1):103–22. 10.1111/j.1469-8137.2007.02346.x PubMed DOI

Beaumont MA, Nichols RA. Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society B-Biological Sciences. 1996;263(1377):1619–26.

Eveno E, Collada C, Guevara MA, Leger V, Soto A, Diaz L, et al. Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Molecular Biology and Evolution. 2008;25(2):417–37. PubMed

Namroud M-C, Beaulieu J, Juge N, Laroche J, Bousquet J. Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Molecular Ecology. 2008;17(16):3599–613. 10.1111/j.1365-294X.2008.03840.x PubMed DOI PMC

Prunier J, Laroche J, Beaulieu J, Bousquet J. Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Molecular Ecology. 2011;20(8):1702–16. 10.1111/j.1365-294X.2011.05045.x PubMed DOI

Holliday JA, Suren H, Aitken SN. Divergent selection and heterogeneous migration rates across the range of Sitka spruce (Picea sitchensis). Proceedings of the Royal Society B-Biological Sciences. 2012;279(1734):1675–83. PubMed PMC

Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: From genotyping to genome typing. Nature Reviews Genetics. 2003;4(12):981–94. PubMed

Hansen MM, Olivieri I, Waller DM, Nielsen EE, Ge MWG. Monitoring adaptive genetic responses to environmental change. Molecular Ecology. 2012;21(6):1311–29. 10.1111/j.1365-294X.2011.05463.x PubMed DOI

Sork VL, Aitken SN, Dyer RJ, Eckert AJ, Legendre P, Neale DB. Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate. Tree Genetics & Genomes. 2013:1–11.

Stinchcombe JR, Hoekstra HE. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity. 2008;100(2):158–70. PubMed

Endler JA. Geographic variation, speciation, and clines. Monographs in population biology. 1977;10:1–246. PubMed

Yeaman S. Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proceedings of the National Academy of Sciences. 2013;110(19):E1743–51. PubMed PMC

Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, Wilczek AM. A Map of Local Adaptation in Arabidopsis thaliana. Science. 2011;334(6052):86–9. 10.1126/science.1209271 PubMed DOI

Schnee FB, Thompson JN. Conditional neutrality of polygene effects. Evolution. 1984;38(1):42–6. PubMed

Hancock AM, Brachi B, Faure N, Horton MW, Jarymowycz LB, Sperone FG, et al. Adaptation to Climate Across the Arabidopsis thaliana Genome. Science. 2011;334(6052):83–6. 10.1126/science.1209244 PubMed DOI

Anderson JT, Willis JH, Mitchell-Olds T. Evolutionary genetics of plant adaptation. Trends in Genetics. 2011;27(7):258–66. 10.1016/j.tig.2011.04.001 PubMed DOI PMC

Pujol B, Wilson AJ, Ross RIC, Pannell JR. Are Q(ST)-F(ST) comparisons for natural populations meaningful? Molecular Ecology. 2008;17(22):4782–5. 10.1111/j.1365-294X.2008.03958.x PubMed DOI

Eckenwalder JE. Systematics and evolution of Populus. Stettler RF B H, Heilman PE, Hinckley TM, editor. National Research Council of Canada Ottawa, ON, Canada: NRC Research Press; 1996.

Cronk QCB. Plant eco-devo: the potential of poplar as a model organism. New Phytologist. 2005;166(1):39–48. PubMed

Carroll A, Somerville C. Cellulosic Biofuels. Annual Review of Plant Biology. 2009;60:165–82. 10.1146/annurev.arplant.043008.092125 PubMed DOI

Sannigrahi P, Ragauskas AJ, Tuskan GA. Poplar as a feedstock for biofuels: A review of compositional characteristics. Biofuels Bioproducts & Biorefining-Biofpr. 2010;4(2):209–26.

Stanton B, Neale D, Li S. Populus breeding: from the classical to the genomic approach In: Jansson S RB, Groover AT, editor. Genetics and Genomics of Populus: Springer; 2010. p. 309–48.

Porth I, El-Kassaby YA. Using Populus as a lignocellulosic feedstock for bioethanol. Biotechnology Journal. 2015;10(4):510–24. 10.1002/biot.201400194 PubMed DOI

Slavov GT, Zhelev P. Salient Biological Features, Systematics, and Genetic Variation of Populus. Genetics and Genomics of Populus. 2010;8:15–38.

Lexer C, Stoelting KN. Whole genome sequencing (WGS) meets biogeography and shows that genomic selection in forest trees is feasible. New Phytologist. 2012;196(3):652–4. 10.1111/j.1469-8137.2012.04362.x PubMed DOI

Slavov GT, Leonardi S, Adams WT, Strauss SH, DiFazio SP. Population substructure in continuous and fragmented stands of Populus trichocarpa. Heredity. 2010;105(4):348–57. 10.1038/hdy.2010.73 PubMed DOI

Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, et al. Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytologist. 2012;196(3):713–25. 10.1111/j.1469-8137.2012.04258.x PubMed DOI

Geraldes A, Difazio SP, Slavov GT, Ranjan P, Muchero W, Hannemann J, et al. A 34K SNP genotyping array for Populus trichocarpa: Design, application to the study of natural populations and transferability to other Populus species. Molecular Ecology Resources. 2013;13(2):306–23. 10.1111/1755-0998.12056 PubMed DOI

Geraldes A, Farzaneh N, Grassa CJ, McKown AD, Guy RD, Mansfield SD, et al. Landscape genomics of Populus trichocarpa: the role of hybridization, limited gene flow, and natural selection in shaping patterns of population structure. Evolution. 2014;68(11):3260–80. 10.1111/evo.12497 PubMed DOI

Porth I, Klápště J, Skyba O, Lai BS, Geraldes A, Muchero W, et al. Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations. New Phytologist. 2013;197(3):777–90. 10.1111/nph.12014 PubMed DOI

La Mantia J, Klapste J, El-Kassaby YA, Azam S, Guy RD, Douglas CJ, et al. Association Analysis Identifies Melampsora xcolumbiana Poplar Leaf Rust Resistance SNPs. PloS One. 2013;8(11):e78423 10.1371/journal.pone.0078423 PubMed DOI PMC

McKown A, Klápště J, Guy R, Geraldes A, Porth I, Hannemann J, et al. Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa. New Phytologist. 2014;203(2):535–53. 10.1111/nph.12815 PubMed DOI

Evans LM, Slavov GT, Rodgers-Melnick E, Martin J, Ranjan P, Muchero W, et al. Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nature genetics. 2014;46(10):1089–96. 10.1038/ng.3075 PubMed DOI

Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G. LOSITAN: A workbench to detect molecular adaptation based on a F(st)-outlier method. BMC Bioinformatics. 2008;9:323 10.1186/1471-2105-9-323 PubMed DOI PMC

Hemani G, Knott S, Haley C. An Evolutionary Perspective on Epistasis and the Missing Heritability. PLoS Genetics 2013;9(2):e1003295 10.1371/journal.pgen.1003295 PubMed DOI PMC

Porth I, Klapšte J, Skyba O, Hannemann J, McKown AD, Guy RD, et al. Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. New Phytologist. 2013;200(3):710–26. 10.1111/nph.12422 PubMed DOI

McKown AD, Guy RD, Quamme L, Klápště J, La Mantia J, Constabel CP, et al. Association genetics, geography and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade-offs. Molecular Ecology. 2014;23(23):5771–90. 10.1111/mec.12969 PubMed DOI

McKown AD, Guy RD, Klápště J, Geraldes A, Friedmann M, Cronk QCB, et al. Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa. New Phytologist. 2014;201(4):1263–76. 10.1111/nph.12601 PubMed DOI

Frentiu FD, Clegg SM, Chittock J, Burke T, Blows MW, Owens IPF. Pedigree-free animal models: the relatedness matrix reloaded. Proceedings of the Royal Society B-Biological Sciences. 2008;275(1635):639–47. PubMed PMC

Ritland K, Ritland C. Inferences about quantitative inheritance based on natural population structure in the yellow monkeyflower, Mimulus guttatus. Evolution. 1996;50(3):1074–82. PubMed

Lippert C, Quon G, Kang EY, Kadie CM, Listgarten J, Heckerman D. The benefits of selecting phenotype-specific variants for applications of mixed models in genomics. Scientific Reports. 2013;3:1815 10.1038/srep01815 PubMed DOI PMC

Lynch M, Walsh B. Genetics and Analysis of Quantitative Traits. first ed. Sunderland, MA, USA: Sinauer Associates; 1998. 980 p.

Jannink J-L. Identifying quantitative trait locus by genetic background interactions in association studies. Genetics. 2007;176(1):553–61. PubMed PMC

Carter AJR, Hermisson J, Hansen TF. The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theoretical Population Biology. 2005;68(3):179–96. PubMed

Kremer A, Le Corre V. Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity. 2012;108(4):375–85. 10.1038/hdy.2011.81 PubMed DOI PMC

Anonymous. On beyond GWAS. Nature Genetics. 2010;42(7):551 10.1038/ng0710-551 PubMed DOI

Epperson BK. Geographical Genetics. Princeton University Press, Princeton, New Jersey; 2003. 376 p.

Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, et al. A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell. 2007;19(8):2370–90. PubMed PMC

Fabbrini F, Gaudet M, Bastien C, Zaina G, Harfouche A, Beritognolo I, et al. Phenotypic plasticity, QTL mapping and genomic characterization of bud set in black poplar. BMC Plant Biology. 2012;12:47 10.1186/1471-2229-12-47 PubMed DOI PMC

Petterle A, Karlberg A, Bhalerao RP. Daylength mediated control of seasonal growth patterns in perennial trees. Current Opinion in Plant Biology. 2013;16(3):301–6. 10.1016/j.pbi.2013.02.006 PubMed DOI

Rohde A, Bastien C, Boerjan W. Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiology. 2011;31(5):472–82. 10.1093/treephys/tpr038 PubMed DOI

Kalcsits LA, Silim S, Tanino K. Warm temperature accelerates short photoperiod-induced growth cessation and dormancy induction in hybrid poplar (Populus x spp.). Trees-Structure and Function. 2009;23(5):971–9.

Hanninen H, Tanino K. Tree seasonality in a warming climate. Trends in Plant Science. 2011;16(8):412–6. 10.1016/j.tplants.2011.05.001 PubMed DOI

Wang Y-Y, Tsay Y-F. Arabidopsis Nitrate Transporter NRT1.9 Is Important in Phloem Nitrate Transport. Plant Cell. 2011;23(5):1945–57. 10.1105/tpc.111.083618 PubMed DOI PMC

Bai H, Euring D, Volmer K, Janz D, Polle A. The Nitrate Transporter (NRT) Gene Family in Poplar. PloS One. 2013;8(8):e72126 10.1371/journal.pone.0072126 PubMed DOI PMC

Duarte JM, Cui LY, Wall PK, Zhang Q, Zhang XH, Leebens-Mack J, et al. Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Molecular Biology and Evolution. 2006;23(2):469–78. PubMed

Camanes G, Pastor V, Cerezo M, Garcia-Andrade J, Vicedo B, Garcia-Agustin P, et al. A Deletion in NRT2.1 Attenuates Pseudomonas syringae-Induced Hormonal Perturbation, Resulting in Primed Plant Defenses. Plant Physiology. 2012;158(2):1054–66. 10.1104/pp.111.184424 PubMed DOI PMC

Himelblau E, Amasino RM. Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. Journal of Plant Physiology. 2001;158(10):1317–23.

Black BL, Fuchigami LH, Coleman GD. Partitioning of nitrate assimilation among leaves, stems and roots of poplar. Tree Physiology. 2002;22(10):717–24. PubMed

Larisch C, Dittrich M, Wildhagen H, Lautner S, Fromm J, Polle A, et al. Poplar Wood Rays Are Involved in Seasonal Remodeling of Tree Physiology. Plant Physiology. 2012;160(3):1515–29. 10.1104/pp.112.202291 PubMed DOI PMC

Chandrashekar M, Heather WA. Temperature sensitivity of reactions of populus spp to races of Melampsora-larici-populina. Phytopathology. 1981;71(4):421–4.

Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R, et al. Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters. 2012;15(4):378–92. 10.1111/j.1461-0248.2012.01746.x PubMed DOI PMC

Le Corre V, Kremer A. The genetic differentiation at quantitative trait loci under local adaptation. Molecular Ecology. 2012;21(7):1548–66. 10.1111/j.1365-294X.2012.05479.x PubMed DOI

Mimura M, Aitken SN. Adaptive gradients and isolation-by-distance with postglacial migration in Picea sitchensis. Heredity. 2007;99(2):224–32. PubMed

Soolanayakanahally RY, Guy RD, Silim SN, Song M. Timing of photoperiodic competency causes phenological mismatch in balsam poplar (Populus balsamifera L.). Plant Cell and Environment. 2013;36(1):116–27. PubMed

Luquez V, Hall D, Albrectsen BR, Karlsson J, Ingvarsson P, Jansson S. Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genetics & Genomes. 2008;4(2):279–92.

Fracheboud Y, Luquez V, Bjorken L, Sjodin A, Tuominen H, Jansson S. The Control of Autumn Senescence in European Aspen. Plant Physiology. 2009;149(4):1982–91. 10.1104/pp.108.133249 PubMed DOI PMC

Howe GT, Hackett WP, Furnier GR, Klevorn RE. Photoperiodic responses of a northern and southern ecotype of black cottonwood. Physiologia Plantarum. 1995;93(4):695–708.

Whitlock MC. Evolutionary inference from Q(ST). Molecular Ecology. 2008;17(8):1885–96. 10.1111/j.1365-294X.2008.03712.x PubMed DOI

Lefèvre F, Boivin T, Bontemps A, Courbet F, Davi H, Durand-Gillmann M, et al. Considering evolutionary processes in adaptive forestry. Annals of Forest Science. 2013:1–17.

Aitken SN, Whitlock MC. Assisted Gene Flow to Facilitate Local Adaptation to Climate Change. Annual Review of Ecology, Evolution, and Systematics. 2013;44:367

Xie C-Y, Ying CC, Yanchuk AD, Holowachuk DL. Ecotypic mode of regional differentiation caused by restricted gene migration: a case in black cottonwood (Populus trichocarpa) along the Pacific Northwest coast. Canadian Journal of Forest Research. 2009;39(3):519–26.

McKown AD, Guy RD, Azam MS, Drewes EC, Quamme LK. Seasonality and phenology alter functional leaf traits. Oecologia. 2013;172(3):653–65. 10.1007/s00442-012-2531-5 PubMed DOI

Porth I, El-Kassaby Y. Assessment of the Genetic Diversity in Forest Tree Populations Using Molecular Markers. Diversity. 2014;6(2):283.

Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403–5. 10.1093/bioinformatics/btn129 PubMed DOI

Schnute JT, Boers NM, Haigh R. PBS mapping 2: User's guide—Introduction. Canadian Technical Report of Fisheries and Aquatic Sciences. 2004;2549:1–V.

Moran PAP. Notes on continuous stochastic phenomena. Biometrika. 1950;37(1–2):17–23. PubMed

Bivand R. Spdep: spatial dependence: weighting schemes, statistics and models. R package version 0.5–77, Available online at http://cran.r-project.org/src/constrib/Descriptions/spdep.html. 2014.

Yang W-Y, Novembre J, Eskin E, Halperin E. A model-based approach for analysis of spatial structure in genetic data. Nature Genetics. 2012;44(6):725–31. 10.1038/ng.2285 PubMed DOI PMC

Wang T, Hamann A, Spittlehouse DL, Murdock TQ. ClimateWNA-High-Resolution Spatial Climate Data for Western North America. Journal of Applied Meteorology and Climatology. 2012;51(1):16–29.

Di Giuseppe E, Jona Lasinio G, Esposito S, Pasqui M. Functional clustering for Italian climate zones identification. Theoretical and Applied Climatology. 2013;114(1–2):39–54.

Saether SA, Fiske P, Kalas JA, Kuresoo A, Luigujoe L, Piertney SB, et al. Inferring local adaptation from Q(ST)-F-ST comparisons: neutral genetic and quantitative trait variation in European populations of great snipe. Journal of Evolutionary Biology. 2007;20(4):1563–76. PubMed

Henderson CR. Applications of Linear Models in Animal Breeding. Guelph, ON: University of Guelph; 1984. 423 p.

VanRaden PM. Efficient Methods to Compute Genomic Predictions. Journal of Dairy Science. 2008;91(11):4414–23. 10.3168/jds.2007-0980 PubMed DOI

Wimmer V, Albrecht T, Auinger HJ, Schön CC. synbreed: a framework for the analysis of genomic prediction data using R. Bioinformatics. 2012;28(15):2086–7. 10.1093/bioinformatics/bts335 PubMed DOI

McKay JK, Latta RG. Adaptive population divergence: markers, QTL and traits. Trends in Ecology & Evolution. 2002;17(6):285–91.

Gilmour AR, Gogel BJ, Cullis BR, Welham SJ, Thompson R. ASReml User Guide Release 1.0. Hemel Hempstead: VSN International Ltd; 2002.

Joost S, Bonin A, Bruford MW, Despres L, Conord C, Erhardt G, et al. A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Molecular Ecology. 2007;16(18):3955–69. PubMed

Lind MI, Ingvarsson PK, Johansson H, Hall D, Johansson F. Gene flow and selection on phenotypic plasticity in an island system of rana temporaria. Evolution. 2011;65(3):684–97. 10.1111/j.1558-5646.2010.01122.x PubMed DOI

Lewontin RC, Krakauer J. Distribution of gene frequency as a test of theory of selective neutrality of polymorphisms. Genetics. 1973;74(1):175–95. PubMed PMC

Whitlock MC, Guillaume F. Testing for Spatially Divergent Selection: Comparing Q(ST) to F-ST. Genetics. 2009;183(3):1055–63. 10.1534/genetics.108.099812 PubMed DOI PMC

Geraldes A, Pang J, Thiessen N, Cezard T, Moore R, Zhao Y, et al. SNP discovery in black cottonwood (Populus trichocarpa) by population transcriptome resequencing. Molecular Ecology Resources. 2011;11(Suppl 1):81–92. 10.1111/j.1755-0998.2010.02960.x PubMed DOI

Adaptive differentiation of Festuca rubra along a climate gradient revealed by molecular markers and quantitative traits

Sexual homomorphism in dioecious trees: extensive tests fail to detect sexual dimorphism in Populus †