Adaptation to complex environments reveals pervasive trade-offs and genomic targets with large pleiotropic effects

Much of our knowledge on the dynamics of adaptation comes from experimental evolution studies that expose populations to a single selective pressure. However, populations in nature rarely adapt to a single stress at a time. Instead, various biotic and abiotic factors come together to produce complex selective environments. Here, we used experimental evolution to describe adaptive dynamics in the presence of simultaneous stressors, and to quantify the evolution of trade-offs between stressors in a complex environment. We adapted populations of the yeast Saccharomyces cerevisiae to a full-factorial combination of four stressors over the course of 15 serial transfers. Rapid fitness increases were accompanied by the accumulation of mutations in genes and pathways related to specific stressors. Trade-offs evolved rapidly, with the order and mode of trade-off evolution varying between environments due to the inherent physiological and genetic basis of resistance to each stressor. Compensatory evolution for maladaptation as a result of initial trade-offs was typically mediated by fine-tuning of genes associated with the initially adapted environmental component, rather than those associated with the maladapted trait. As environmental complexity increased, mutations had increasingly broader effects across multiple biological processes. Although shared mutations at the individual SNP level were rare, recurrent mutations affecting the same genes and putative biological processes were abundant across environmental complexity. Our results suggest that adaptation in complex environments follows genetic trajectories shaped by pleiotropy and trade-offs, but these trajectories may impose lasting constraints on future adaptation.