Decoding the architecture of living systems

Abstract

The possibility that evolutionary forces—together with a few fundamental factors such as thermodynamic constraints, specific computational features enabling information processing, and ecological processes—might constrain the logic of living systems is tantalizing. However, it is often overlooked that any practical implementation of such a logic requires complementary circuitry that, in biological systems, happens through complex networks of genetic regulation, metabolic reactions, cellular signaling, communication, social and eusocial non-trivial organization. Here, we review and discuss how circuitries are not merely passive structures, but active agents of change that, by means of hierarchical and modular organization, are able to enhance and catalyze the evolution of evolvability. By analyzing the role of non-trivial topologies in major evolutionary transitions under the lens of statistical physics and nonlinear dynamics, we show that biological innovations are strictly related to circuitry and its deviation from trivial structures and (thermo)dynamic equilibria. We argue that sparse heterogeneous networks such as hierarchical modular, which are ubiquitously observed in nature, are favored in terms of the trade-off between energetic costs for redundancy, error-correction and maintenance. We identify three main features—namely, interconnectivity, plasticity and interdependency—pointing towards a unifying framework for modeling the phenomenology, discussing them in terms of dynamical systems theory, non-equilibrium thermodynamics and evolutionary dynamics. Within this unified picture, we also show that ‘slow’ evolutionary dynamics is an emergent phenomenon governed by the replicator-mutator equation as the direct consequence of a constrained variational nonequilibrium process. Overall, this work highlights how dynamical systems theory and nonequilibrium thermodynamics provide powerful analytical techniques to study biological complexity.