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Physical foundations of biological complexity

Yuri I. Wolf, Mikhail I. Katsnelson, and Eugene V. Koonin
PNAS September 11, 2018 115 (37) E8678-E8687; published ahead of print August 27, 2018 https://doi.org/10.1073/pnas.1807890115
Yuri I. Wolf
aNational Center for Biotechnology Information, National Library of Medicine, Bethesda, MD 20894;
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Mikhail I. Katsnelson
bInstitute for Molecules and Materials, Radboud University, 6525AJ Nijmegen, The Netherlands
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Eugene V. Koonin
aNational Center for Biotechnology Information, National Library of Medicine, Bethesda, MD 20894;
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  • ORCID record for Eugene V. Koonin
  • For correspondence: koonin@ncbi.nlm.nih.gov
  1. Contributed by Eugene V. Koonin, July 31, 2018 (sent for review May 21, 2018; reviewed by Sergei Maslov and Eörs Szathmáry)

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Significance

Living organisms are characterized by a degree of hierarchical complexity that appears to be inaccessible to even the most complex inanimate objects. Routes and patterns of the evolution of complexity are poorly understood. We propose a general conceptual framework for emergence of complexity through competing interactions and frustrated states similar to those that yield patterns in striped glasses and cause self-organized criticality. We show that biological evolution is replete with competing interactions and frustration that, in particular, drive major transitions in evolution. The key distinction between biological and nonbiological systems seems to be the existence of long-term digital memory and phenotype-to-genotype feedback in living matter.

Abstract

Biological systems reach hierarchical complexity that has no counterpart outside the realm of biology. Undoubtedly, biological entities obey the fundamental physical laws. Can today’s physics provide an explanatory framework for understanding the evolution of biological complexity? We argue that the physical foundation for understanding the origin and evolution of complexity can be gleaned at the interface between the theory of frustrated states resulting in pattern formation in glass-like media and the theory of self-organized criticality (SOC). On the one hand, SOC has been shown to emerge in spin-glass systems of high dimensionality. On the other hand, SOC is often viewed as the most appropriate physical description of evolutionary transitions in biology. We unify these two faces of SOC by showing that emergence of complex features in biological evolution typically, if not always, is triggered by frustration that is caused by competing interactions at different organizational levels. Such competing interactions lead to SOC, which represents the optimal conditions for the emergence of complexity. Competing interactions and frustrated states permeate biology at all organizational levels and are tightly linked to the ubiquitous competition for limiting resources. This perspective extends from the comparatively simple phenomena occurring in glasses to large-scale events of biological evolution, such as major evolutionary transitions. Frustration caused by competing interactions in multidimensional systems could be the general driving force behind the emergence of complexity, within and beyond the domain of biology.

  • evolution of complexity
  • competing interactions
  • frustrated states
  • spin glasses
  • self-organized criticality

Footnotes

  • ↵1To whom correspondence should be addressed. Email: koonin{at}ncbi.nlm.nih.gov.
  • Author contributions: Y.I.W., M.I.K., and E.V.K. designed research; Y.I.W., M.I.K., and E.V.K. performed research; and M.I.K. and E.V.K. wrote the paper.

  • Reviewers: S.M., University of Illinois at Urbana–Champaign; and E.S., MTA Ecological Research Center.

  • The authors declare no conflict of interest.

  • Copyright © 2018 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Physical foundations of biological complexity
Yuri I. Wolf, Mikhail I. Katsnelson, Eugene V. Koonin
Proceedings of the National Academy of Sciences Sep 2018, 115 (37) E8678-E8687; DOI: 10.1073/pnas.1807890115

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Physical foundations of biological complexity
Yuri I. Wolf, Mikhail I. Katsnelson, Eugene V. Koonin
Proceedings of the National Academy of Sciences Sep 2018, 115 (37) E8678-E8687; DOI: 10.1073/pnas.1807890115
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  • Article
    • Abstract
    • Glasses, Patterns, Frustrated States, and SOC
    • Competing Interactions and Frustrated States as Drivers of Biological Evolution
    • Evolutionary Transitions and Major Innovations Driven by Competing Interactions
    • Cancer, Aging, and Death
    • Frustration as the Key Factor Underlying All Complexity in Nature and the Specifics of Biological Evolution
    • Acknowledgments
    • Footnotes
    • References
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