TY - JOUR
T1 - Evolutionary transitions in controls reconcile adaptation with continuity of evolution
AU - Badyaev, Alexander V.
N1 - Funding Information:
I am grateful to three referees for insightful comments that improved the paper, to Vincent Debat and Arnaud Le Rouzic for the invitation to contribute, suggestions of important references, and editorial comments, and to Renee Duckworth, Xander Posner, Erin Morrison, and Nikolay Formozov for helpful discussion. Empirical work on evolution of avian carotenoid network was funded by the grants from the National Science Foundation ( DEB-0075388 , IBN-0218313 , and DEB-0077804 ) and the David and Lucille Packard Fellowship.
Publisher Copyright:
© 2018 Elsevier Ltd
PY - 2019/4
Y1 - 2019/4
N2 - 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.
AB - 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.
KW - Controllability
KW - Degeneracy
KW - Evolvability
KW - Innovation
KW - Metabolic network
KW - Robustness
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U2 - 10.1016/j.semcdb.2018.05.014
DO - 10.1016/j.semcdb.2018.05.014
M3 - Review article
C2 - 29778791
AN - SCOPUS:85044067204
SN - 1084-9521
VL - 88
SP - 36
EP - 45
JO - Seminars in Cell and Developmental Biology
JF - Seminars in Cell and Developmental Biology
ER -