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.