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.

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 Forest and Conservation Sciences University of British Columbia Vancouver BC V6T 1Z4 Canada Corn Soybean and Wheat Quality Research Unit United States Department of Agriculture Wooster Ohio 44691 United States of America

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