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

Alexander V. Badyaev, Erin S. Morrison

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)647-662
Number of pages16
JournalEvolution
Volume72
Issue number3
DOIs
StatePublished - Mar 2018

Keywords

  • Age
  • degeneracy
  • evolvability
  • network
  • phenotypic flexibility
  • robustness

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Agricultural and Biological Sciences(all)

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