Emergent buffering balances evolvability and robustness in the evolution of phenotypic flexibility

Evolution of adaptive phenotypic flexibility requires a system that can dynamically restore and update a functional phenotype in response to environmental change. The architecture of such a system evolves under the conflicting demands of versatility and robustness, and resolution of these demands should be particularly evident in organisms that require external inputs for reiterative trait production within a generation, such as in metabolic networks that underlie yearly acquisition of diet‐dependent coloration in birds. Here, we show that a key structural feature of carotenoid networks–redundancy of biochemical pathways–enables these networks to translate variable environmental inputs into consistent phenotypic outcomes. We closely followed life‐long changes in structure and utilization of metabolic networks in a large cohort of free‐living birds and found that greater individual experience with dietary change between molts leads to wider occupancy of the metabolic network and progressive accumulation of redundant pathways in a functionally active network. This generated a regime of emergent buffering whereby greater dietary experience was mechanistically linked to greater robustness of resulting traits and an increasing ability to retain and implement previous adaptive solutions. Thus, experience‐related buffering links evolvability and robustness in carotenoid‐metabolizing networks and we argue that this mechanistic principle facilitates the evolution of phenotypic flexibility.