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

Abstract

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.

Structure versus time in the evolutionary diversification of avian carotenoid metabolic networks

“…Lu & Li, 2008). Frequent and reversible utilization of distinct biochemical modules in avian evolution (Morrison & Badyaev, 2016a;Badyaev & Morrison, 2018), along with the evolutionary conservation of modules comprising of derived carotenoids reachable from a diverse array of dietary precursors (Badyaev et al, 2015), could further maintain access to the same biochemical network during evolution.…”

Phenotypic Plasticity & Evolution

“…In general, to achieve stability at a higher level of organization, the lower scale entities must be in constant action-modifying their behavior and interactions in response to environmental changes. Hence, robust systems maintain a dynamic stability with builtin flexibility that tracks and responds to internal and external changes to maintain a steady output (Nijhout and Reed 2014;Badyaev and Morrison 2018). Behavioral responses and interactions at all biological scales, from molecular interactions and physiological controls to organismal and ecosystem homeostasis, are at the forefront of how systems maintain robustness in the face of environmental change.…”

Generic model for biological regulation

“…Emergence is an explanation when behaviour of a complex system containing many interactions between system components cannot be attributed to the sum of the components. Emergent processes have been identi ed in a wide range of biological phenomena, such as quorum sensing in bacterial colonies [8], robustness of biological processes [9,10], evolution of biological exibility [11], and synthetic biology [12].…”