Climatic niche predicts the landscape structure of locally adaptive standing genetic variation

Abstract

Within a species range, intraspecific diversity in the form of adaptive standing genetic variation (SGV) may be non-randomly clustered into different geographic regions, reflecting the combined effects of historical range movements and spatially-varying natural selection. As a consequence of a patchy distribution of adaptive SGV, populations in different parts of the range are likely to vary in their capacity to respond to changing selection pressures, especially long-lived sessile organisms like forest trees. However, the spatial distribution of adaptive SGV across the landscape is rarely considered when predicting species responses to environmental change. Here, we use a landscape genomics approach to estimate the distribution of adaptive SGV along spatial gradients reflecting the expansion history and contemporary climatic niche of balsam poplar, Populus balsamifera (Salicaceae), a widely distributed forest tree with a transcontinental distribution in North America. By scanning the genome for signatures of spatially varying local adaptation, we estimated how adaptive SGV has been shaped by geographic distance from the rear range edge (expansion history) versus proximity to the current center of the climatic niche (environmental selection). We found that adaptive SGV was strongly structured by the current climatic niche, with surprisingly little importance attributable to historical effects such as migration out of southern refugia. As expected, the effect of the climatic niche on SGV was strong for genes whose expression is responsive to abiotic stress (drought), although genes upregulated under biotic (wounding) stress also contained SGV that followed climatic and latitudinal gradients. The latter result could reflect parallel selection pressures, or co-regulation of functional pathways involved in both abiotic and biotic stress responses. Our study in balsam poplar suggests that clustering of locally adaptive SGV within ranges primarily reflects spatial proximity within the contemporary climatic niche - an important consideration for the design of effective strategies for biodiversity conservation and avoidance of maladaptation under climate change.