Physical foundations of biological complexity

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.