View Program - 2022 Population, Evolutionary, and Quantitative Genetics Conference

Building a genotype-phenotype-fitness map of adaptation is a central goal in evolutionary biology. Despite the importance of building such a map, it is difficult to do so even when adaptive mutations are known because it is hard to enumerate which phenotypes make these mutations adaptive. We address this problem by first quantifying how the fitness of hundreds of adaptive yeast mutants responds to subtle environmental shifts. We then model the number of phenotypes these mutations collectively influence by decomposing these patterns of fitness variation. We find that a small number of inferred phenotypes can predict fitness of the adaptive mutations near their original glucose-limited evolution condition. Importantly, inferred phenotypes that matter little to fitness at or near the evolution condition can matter strongly in distant environments. This suggests that adaptive mutations are locally modular — affecting a small number of phenotypes that matter to fitness in the environment where they evolved — yet globally pleiotropic — affecting additional phenotypes that may reduce or improve fitness in new environments. By isolating additional mutations from further evolution experiments and studying their fitness effects in subtle environmental perturbations both near and far from their original evolution condition, we further demonstrate that adaptive mutations indeed affect only a small number of phenotypes that contribute to fitness only in the environment in which they evolved but have diverse effects in distant environments. Using these approaches, we also show that further adaptive steps depend on the specific phenotypic effects of initial mutations, showcasing that directional selection alone can generate a large amount of latent phenotypic diversity with substantial effects on further adaptive evolution.

Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation