Pleiotropic consequences of adaptation across gradations of environmental stress in budding yeast

Adaptation to one environment often results in fitness gains and losses in other conditions. To characterize how these consequences of adaptation depend on the physical similarity between environments, we evolved 180 populations of Saccharomyces cerevisiae at different degrees of stress induced by either salt, temperature, pH, or glucose depletion. We measure how the fitness of clones adapted to each environment depends on the intensity of the corresponding type of stress. We find that clones evolved in a given type and intensity of stress tend to gain fitness in other similar intensities of that stress, and lose progressively more fitness in more physically dissimilar environments. These fitness trade-offs are asymmetric: adaptation to permissive conditions incurred a smaller trade-off in stressful conditions than vice versa. We also find that fitnesses of clones are highly correlated across similar intensities of stress, but these correlations decay towards zero in more dissimilar environments. To interpret these results, we introduce the concept of a joint distribution of fitness effects of new mutations in multiple environments (the JDFE), which describes the probability that a given mutation has particular fitness effects in some set of conditions. We find that our observations are consistent with JDFEs that are highly correlated between physically similar environments, and that become less correlated and asymmetric as the environments become more dissimilar. The JDFE provides a framework for quantifying evolutionary similarity between conditions, and forms a useful basis for theoretical work aimed at predicting the outcomes of evolution in fluctuating environments.