Adaptation to complex environments is associated with higher fitness costs under benign conditions

Complex environments with simultaneous change in multiple stressors is the new norm in ecosystems worldwide, and adaptive evolution will be critical for population persistence under these combined environmental challenges. Yet, how the selective complexity imposed by such stressor combinations affects the pace of evolution remains poorly understood. Using a coordinated experiment, we exposed 14 species, from bacteria to unicellular eukaryotes and plants, to single stressors versus their pairwise combinations over multiple generations, while keeping the overall stress level comparable. We find that populations evolving under combined stressors tended to have lower fitness increase, and a shallower relation between initial maladaptation and fitness gain, than populations evolving under single stressors, although this direct response depended strongly on stressor type. When assayed in the control, benign conditions, lines evolved under combined stressors had higher fitness reductions than those evolved under single stressors, with higher consistency between species than for direct evolutionary responses. Our unique coordinated experimental evolution approach provides new insights into how environmental complexity can impact the pace of evolution, together with revealing the diversity of these responses. It further highlights the importance of incorporating evolutionary dynamics into the combined-stressor research agenda.