Adaptive differentiation of traits and underlying loci can occur at a small geographic scale if natural selection is stronger than gene flow and drift. We investigated this hypothesis using coupled quantitative genetic and genomic approaches for a wind-pollinated tree species, Quercus rubra, along the steep, narrow gradient of the Lake Superior coast that encompasses four USDA Hardiness Zones within 100 km. For the quantitative genetic component, we examined phenotypic differentiation among eight populations in a common garden. For the genomic component, we quantified genetic differentiation for 26 populations using RAD-seq. Because hybridization with the congener Quercus ellipsoidalis has been documented elsewhere, we also included two populations of this species for comparison. In the common garden study, we found a strong signal of population differentiation that was significantly associated with at least one climate factor for nine of ten measured traits. In contrast, we found no evidence of genomic differentiation among populations based on FST or other measures. However, distance-based, and genotype-environment association analyses identified loci showing the signature of selection, with one locus in common across five analyses. This locus was associated with the minimum temperature of the coldest month, a climate factor was also significant in the common garden analyses. In addition, we documented introgression from Q. ellipsoidalis into Q. rubra, with rates of introgression correlated with the climate gradient. In sum, this study reveals signatures of selection at the quantitative trait and genomic level consistent with climate adaptation occurring at a small geographic scale.

Adaptive differentiation in functional traits and their underlying loci can occur across a small geographic area if natural selection is stronger than the countervailing effects of gene flow and drift. We investigated this hypothesis in a long-lived, wind-pollinated species, Quercus rubra, across a fine spatial scale with a steep climate gradient. We examined phenotypic differentiation in a common garden study with eight populations sampled 0-160 km from the coast of Lake Superior. We estimated genomic differentiation for these and 22 additional populations from the same region, along with two populations of a congener, Quercus ellipsoidalis, using RAD-seq. We found a strong signal of population differentiation associated with climate in the common garden study, and differentiation was significantly associated with at least one climate factor for nine of ten measured traits. At the genomic level, we discovered widespread introgression from Q. ellipsoidalis into Q. rubra that increased with distance from the lake. Pairwise FST among Q. rubra populations was low, but both distance-based and environmental association analyses identified loci under selection, with one locus in common across all analyses (CalS10/GSL8). This locus was associated with the precipitation of the driest month, a climate factor that was also significant in the common garden analyses. In sum, this study reveals signatures of selection at the phenotypic and genomic level consistent with climate adaptation, a pattern that is usually seen across a much broader geographic scale.