Abstract
Mutations that a population accumulates during evolution in one (“home”) environment may cause fitness gains or losses in other conditions. Such “pleiotropic” fitness effects shape 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 difference between selection pressures in different environments. To address this question, we evolved 20 replicate populations of the yeast Saccharomyces cerevisiae in 11 laboratory environments and measured their fitnesses across multiple other conditions. We found that evolution in all home environments led to a diversity of patterns of pleiotropic fitness gains and losses, driven by multiple types of mutations. Both generalists and specialists evolved in almost all home environments. Nevertheless, individuals evolved in the same home environment were more phenotypically and genetically similar to each other than to individuals evolved in different conditions. The average pleiotropic fitness increment of a population was smaller (and more negative) in conditions less similar to its home environment. To explain our observations, we propose a model which we call “opportunity-cost pleiotropy”, a generalization of both the “mutation accumulation” and the “antagonistic pleiotropy” models. Our results indicate that the intrinsic randomness of evolutionary dynamics can play as important a role in determining the patterns of pleiotropy as the deterministic differences in selection pressures between environments.