Rapid and exceptionally small-scale adaptation of the alpine plant Cardamine resedifolia to mining-contaminated soils in multi-stress condition.

The mechanisms by which plants tolerate soil contamination have been studied in details in controlled laboratory conditions, but they still remain largely unexplored in natural conditions where mixtures of contaminants are present in soils and their effects might interact with other environmental variables. This is especially true in high-altitude alpine environments, where abiotic stress is naturally heightened, but which so far have received little attention in environmental pollution studies. As we were interested in the tolerance mechanisms at play on very fine spatiotemporal scales for alpine plants growing under multi-stress conditions, we chose Cardamine resedifolia as our biological model. This plant is indeed frequently found in areas contaminated by Trace Metals and Metalloids and Polycyclic Aromatic Hydrocarbons in high elevation. We studied populations from former copper, silver-lead, and coal mines in alpine environments, along with populations growing on nearby reference soils. We measured genetic variability within populations as well as genetic differentiation between them, and tested for local adaptation to soil contamination using reciprocal transplants. Population pairs showing signs of local adaptation were then examined using genome scans to identify genes potentially under selection. We found high levels of genetic differentiation between populations growing on contaminated and reference soils a few dozen meters apart. In most cases local adaptation was detected, especially in former copper mines. Genome scans identified genes involved in metal stress management as potentially being under selection. This study provides evidence for rapid adaptation to human-induced pollution in alpine plants at remarkably small spatial scales. It offers new insights into the short-term ecological and evolutionary consequences of mining activities in alpine ecosystems, particularly in relation to substrate-driven differentiation.