Evolutionary rescue in toxic combinations of metal is dependent on metal interactions

Abstract

Populations facing abrupt environmental change may avoid extinction through evolutionary rescue, in which beneficial mutations allow individuals to survive and reproduce under otherwise lethal conditions. However, theory on evolutionary rescue has largely focused on single stressors, leaving open how interactions among simultaneous stressors shape adaptation. In particular, synergistic interactions, which amplify toxicity, and antagonistic interactions, which reduce it, may impose distinct selective pressures and lead to different fitness outcomes. To investigate this, we experimentally evolved Saccharomyces cerevisiae under lethal combinations of six metals (Cd, Co, Cu, Mn, Ni, and Zn), obtaining rescued lines in eight of the fifteen pairwise combinations. We then measured the fitness of evolved lines in the original metal combination, each component metal individually, and the ancestral environment. Adaptation differed systematically with metal interactions: lines evolved in antagonistic combinations generally gained fitness in the individual metals as well as in the combination, whereas lines evolved in synergistic combinations tended to show more specialized adaptation, with fitness benefits concentrated in the combination and reduced fitness in the component metals. No rescue was observed in combinations whose toxicity was consistent with concentration addition, although differences in the precise toxicity of experimental treatments may have influenced rescue outcomes. These findings demonstrate that interactions among simultaneous stressors can shape not only the likelihood of evolutionary rescue but also the breadth of its fitness benefits, highlighting the importance of accounting for stressor interactions when investigating evolutionary responses to environmental change.