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

Abstract

Building a genotype-phenotype-fitness map of adaptation is a central goal in evolutionary biology. It is difficult 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.

Hidden paths to endless forms most wonderful: Ecology latently shapes evolution of multicellular development in predatory bacteria

“…See Freund et al 30 for elaboration on use of the term ‘latent-phenotype evolution’ (LPE). Similar terminology has also been used recently by Kinsler et al 31 .…”

“…The likely contributions of LPE to long-term evolutionary processes have been receiving increasing attention [29][30][31][32][33]36 . The outcomes of MyxoEE-3 reported here suggest that not only LPE per se, but the ecological context in which LPE originates, may often be important for the evolution of many developmental systems.…”

“…adaptation or genetic drift) while the actual phenotype is only first manifested, and thus revealed to potential selection, after later exposure to an inductive environment. Such evolution of initially latent phenotypes -latent-phenotype evolution (LPE 29,30 , see Semantics in Methods) -is common [29][30][31][32][33] contributes to evolutionary diversification 29,30 and can fuel some forms of exaptation 26,[34][35][36] .…”

Predicting the fitness costs of complex mutations

“…Finally, the fact that only a subset of the genes influenced by a complex mutation contributes to fitness appears to subscribe to a model in which extended phenotypic pleiotropy and fitness-relevant modularity coexist (Kinsler et al 2020). Thus, we notice that many genes –molecular phenotypes– can be affected by these mutations implying extended phenotypic pleiotropy, like that also suggested by genome-wide association studies (Visscher and Yang 2016).…”

Resource uptake and the evolution of moderately efficient enzymes

“…This framework could even be enriched by other dimensions relevant to the genotype-phenotype-fitness map (Bershtein et al, 2017;Echave, 2019;Kinsler et al, 2020).…”