Divergent Selection in a Mediterranean Pine on Local Spatial Scales

1. The effects of selection on an organism's genome are hard to detect on small spatial scales, as gene flow can swamp signatures of local adaptation. Therefore, most genome scans to detect signatures of environmental selection are performed on large spatial scales; however, divergent selection on the local scale (e.g. between contrasting soil conditions) has also been demonstrated, in particular for herbaceous plants.2. Here, we hypothesised that in topographically complex landscapes, microenvironment variability is strong enough to leave a selective footprint in the genomes of long-lived organisms. To test this, we investigated paired south- versus north-facing Pinus pinaster stands on the local scale, with trees growing in close vicinity (<= 820 m distance between paired south- and north-facing stands), in a Mediterranean mountain area. While trees on north-facing slopes experience less radiation, trees on south-facing slopes suffer from especially harsh conditions, particularly during the dry summer season.3. Two outlier analyses consistently revealed five putatively adaptive loci (out of 4034), in candidate genes two of which encoded non-synonymous substitutions. Additionally, one locus showed consistent allele frequency differences in all three stand pairs indicating divergent selection despite high gene flow on the local scale. Permutation tests demonstrated that our findings were robust.4. Functional annotation of these candidate genes revealed biological functions related to abiotic stress response, such as water availability, in other plant species.5. Synthesis. Our study highlights how divergent selection in heterogeneous microenvironments shapes and maintains the functional genetic variation within populations of long-lived forest tree species, being the first to focus on adaptive genetic divergence between south- and north-facing slopes within continuous forest stands. This is especially relevant in the current context of climate change, as this variation is at the base of plant population responses to future climate.