A minimal scenario for the origin of non-equilibrium order

TL;DR

This paper demonstrates that non-equilibrium order can evolve through selection for speed in models of DNA replication and self-assembly, suggesting that such order may arise before it becomes functionally advantageous.

Contribution

It introduces a general framework showing how error correction mechanisms can evolve via selection for replication speed, even without direct functional benefits.

Findings

Error correction mechanisms can evolve through selection for fast replication.

A 'order through speed' effect is predicted when replication time distribution is broad.

Results are supported by mutational screens of proofreading polymerases.

Abstract

Life uses non-equilibrium mechanisms to create ordered structures not attainable at equilibrium; the resulting order is assumed to provide functional benefits that outweigh costs of time and energy needed by these mechanisms. Here, we show that models of DNA replication and self-assembly, when expanded to include known stalling effects, can evolve error correcting mechanisms like kinetic proofreading and dynamic instability through selection for fast replication alone. We abstract these results into a general framework that predicts a counterintuitive ''order through speed'' effect if the distribution of replication times is wide enough. We test our results against recent mutational screens of proofreading polymerases. Our work suggests the intriguing possibility that non-equilibrium order can evolve even before that order is directly functional, with consequences for the evolution of mutation rates, viral capsid assembly, and the origin of life.