• New York Academy of Sciences
  • Science Sessions: The PNAS Podcast Program

Information-based fitness and the emergence of criticality in living systems

  1. Amos Maritanb,2
  1. Edited* by William Bialek, Princeton University, Princeton, NJ, and approved May 27, 2014 (received for review October 12, 2013)

Significance

Recently, evidence has been mounting that biological systems might operate at the borderline between order and disorder, i.e., near a critical point. A general mathematical framework for understanding this common pattern, explaining the possible origin and role of criticality in living adaptive and evolutionary systems, is still missing. We rationalize this apparently ubiquitous criticality in terms of adaptive and evolutionary functional advantages. We provide an analytical framework, which demonstrates that the optimal response to broadly different changing environments occurs in systems organizing spontaneously—through adaptation or evolution—to the vicinity of a critical point. Furthermore, criticality turns out to be the evolutionary stable outcome of a community of individuals aimed at communicating with each other to create a collective entity.

Abstract

Empirical evidence suggesting that living systems might operate in the vicinity of critical points, at the borderline between order and disorder, has proliferated in recent years, with examples ranging from spontaneous brain activity to flock dynamics. However, a well-founded theory for understanding how and why interacting living systems could dynamically tune themselves to be poised in the vicinity of a critical point is lacking. Here we use tools from statistical mechanics and information theory to show that complex adaptive or evolutionary systems can be much more efficient in coping with diverse heterogeneous environmental conditions when operating at criticality. Analytical as well as computational evolutionary and adaptive models vividly illustrate that a community of such systems dynamically self-tunes close to a critical state as the complexity of the environment increases while they remain noncritical for simple and predictable environments. A more robust convergence to criticality emerges in coevolutionary and coadaptive setups in which individuals aim to represent other agents in the community with fidelity, thereby creating a collective critical ensemble and providing the best possible tradeoff between accuracy and flexibility. Our approach provides a parsimonious and general mechanism for the emergence of critical-like behavior in living systems needing to cope with complex environments or trying to efficiently coordinate themselves as an ensemble.

Footnotes

  • Author contributions: J.H., J.G., S.S., M.A.M., J.R.B., and A.M. designed research; J.H., J.G., and S.S. performed research; and J.H., J.G., S.S., M.A.M., J.R.B., and A.M. wrote the paper.

  • The authors declare no conflict of interest.

  • *This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1319166111/-/DCSupplemental.