Self-organizing physical and biochemical interactions explain diverse behaviours in Physarum polycephalum

Abstract

How can simple organisms lacking nervous systems encode and transmit environmental signals to generate complex, adaptive behaviours? Using the unicellular organism Physarum polycephalum as a model, we identify a unifying mechanochemical mechanism that links intracellular calcium oscillations to large-scale behavioural coordination. We first demonstrate experimentally that local perturbation of the actomyosin cortex is sufficient to induce symmetry breaking and directed migration, even in the absence of nutrient cues. Building on evidence linking calcium concentration to actin depolymerization and contractile relaxation, we develop a mechanochemical tubule model in which self-sustained calcium oscillations are coupled to pressure-driven mechanics. We show that environmental cues, encoded through the local modulation of these oscillations, give rise to directed transport and the redistribution of biomass. By extending this framework to a two-dimensional phase-field model, we demonstrate that this mechanism is sufficient to generate a diverse set of slime mould behaviours, including chemotaxis, network formation, and balancing exploration-exploitation trade-offs. In doing so, we provide a single mechanistic framework linking intracellular dynamics to organism-scale behaviour across spatial and temporal scales. Our work shows that these sophisticated behaviours can emerge from the modulation of self-sustained oscillations coupled by diffusion, providing a physically grounded mechanism for information processing in non-neural organisms and offering insight into the evolutionary origins of coordinated behaviour.