Abstract
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.
Merging quantitative genetics and population genomics, 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. 29,354 SNPs were investigated employing three different outlier detection methods.
Narrow-sense QST for 53% of distinct field QST 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. We highlight that important loci underlying adaptive trait variation also show relationship to climate of origin.
Author summary Comparisons between population differentiation on the basis of quantitative traits and neutral genetic markers inform about the importance of natural selection, genetic drift and gene flow for local adaptation of populations. 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. Marker-inferred relatedness was estimated to obtain the narrow-sense estimate of population differentiation in wild populations. We analyzed an unstructured population of common garden grown Populus trichocarpa individuals to uncover different extents of variation for a suite of field traits, wood quality and pathogen resistance with temperature and precipitation. We consider our approach the most comprehensive, as it uncovers the molecular mechanisms of adaptation using multiple methods and tests. We 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.
