Evolutionary transitions in controls reconcile adaptation with continuity of evolution

• Published in: Seminars in cell & developmental biology 2019-04, Vol.88, p.36-45
• Main Author: Badyaev, Alexander V.
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; Animals; Biological Evolution; Controllability; Degeneracy; Developmental Biology; Epigenesis, Genetic; Evolvability; Gene Regulatory Networks; Gene-Environment Interaction; Genetic Variation; Genotype; Humans; Innovation; Metabolic network; Metabolic Networks and Pathways - genetics; Models, Genetic; Morphogenesis - genetics; Phenotype; Robustness; Selection, Genetic
• ISSN: 1084-9521; 1096-3634
• DOI: 10.1016/j.semcdb.2018.05.014

Evolution proceeds by accumulating functional solutions, necessarily forming an uninterrupted lineage from past solutions of ancestors to the current design of extant forms. At the population level, this process requires an organismal architecture in which the maintenance of local adaptation does not preclude the ability to innovate in the same traits and their continuous evolution. Representing complex traits as networks enables us to visualize a fundamental principle that resolves tension between adaptation and continuous evolution: phenotypic states encompassing adaptations traverse the continuous multi-layered landscape of past physical, developmental and functional associations among traits. The key concept that captures such traversing is network controllability – the ability to move a network from one state into another while maintaining its functionality (reflecting evolvability) and to efficiently propagate information or products through the network within a phenotypic state (maintaining its robustness). Here I suggest that transitions in network controllability – specifically in the topology of controls – help to explain how robustness and evolvability are balanced during evolution. I will focus on evolutionary transitions in degeneracy of metabolic networks – a ubiquitous property of phenotypic robustness where distinct pathways achieve the same end product – to suggest that associated changes in network controls is a common rule underlying phenomena as distinct as phenotypic plasticity, organismal accommodation of novelties, genetic assimilation, and macroevolutionary diversification. Capitalizing on well understood principles by which network structure translates into function of control nodes, I show that accumulating redundancy in one type of network controls inevitably leads to the emergence of another type of controls, forming evolutionary cycles of network controllability that, ultimately, reconcile local adaptation with continuity of evolution.