Chance and Necessity in the Pleiotropic Consequences of Adaptation for Budding Yeast

Mutations that a population accumulates during evolution in one (“home”) environment may cause fitness gains or losses in other conditions. Such pleiotropic fitness effects determine the evolutionary fate of the population in variable environments and can lead to ecological specialization. It is unclear how the pleiotropic outcomes of evolution are shaped by the intrinsic randomness of the evolutionary process and by the deterministic variation in selection pressures across environments. To address this question, we evolved 20 replicate populations of the yeast Saccharomyces cerevisiae in 11 laboratory environments and measured their fitness across multiple conditions. We found that evolution led to diverse pleiotropic fitness gains and losses, driven by multiple types of mutations. Approximately 60% percent of this variation is explained by a clone’s home environment and the most common parallel genetic changes, while about 40% is attributed to the stochastic accumulation of mutations whose pleiotropic effects are unpredictable. While populations typically specialized to their home environment, generalists also evolved in almost all conditions. Our results suggest that the mutations accumulating during evolution incur a variety of pleiotropic costs and benefits with different probabilities. Therefore, whether a population evolves towards a specialist or a generalist phenotype is heavily influenced by chance.