Brief Description
Cooperative behavior in organisms often permits groups to achieve collective tasks that are unattainable to individuals. Such is the case of fire ant workers that aggregate together to create buoyant rafts that unify their colonies and ensure survival during floods. Under certain conditions, these rafts undergo a process called treadmilling that allows them to morph perpetually over the span of several hours. This morphogenesis includes the growth of tether-like protrusions that colonies can use as land-bridges to escape water. Employing a discrete, agent-based model, we here demonstrate how the local interactions between ants in these systems may be sufficient to cause stochastic and spontaneous protrusion emergence in the absence of external gradients, long-range interactions, or targeted stimuli.
Abstract
Collective living systems regularly achieve cooperative emergent functions that individual organisms could not accomplish alone. The rafts of聽fire ants聽(Solenopsis invicta) are often studied in this context for their ability to create aggregated structures comprised entirely of their own bodies, including tether-like protrusions that facilitate exploration of and escape from flooded environments. While similar protrusions are observed in cytoskeletons and cellular aggregates, they are generally dependent on morphogens or external gradients leaving the isolated role of local interactions poorly understood. Here we demonstrate through an ant-inspired, agent-based numerical model how protrusions in ant rafts may emerge spontaneously due to local interactions. The model is comprised of a condensed structural network of agents that represents the monolayer of interconnected worker ants, which floats on the water and gives ant rafts their form. Experimentally, this layer perpetually contracts, which we capture through the pairwise contraction of all neighboring structural agents at a strain rate of d. On top of the structural layer, we model a dispersed, on-lattice layer of motile agents that represents free ants, which walk on top of the floating network. Experimentally, these self-propelled free ants walk with some mean persistence length and speed that we capture through an ant-inspired phenomenological model. Local interactions occur between neighboring free ants within some radius of detection, R, and the persistence length of freely active agents is tuned through a noise parameter, [eta] as introduced by the Vicsek model. Both R and [eta] where fixed to match the experimental trajectories of free ants. Treadmilling of the raft occurs as agents transition between the structural and free layers in accordance with experimental observations. Ultimately, we demonstrate how phases of exploratory protrusion growth may be induced by increased ant activity as characterized by a dimensionless parameter, A. These results provide an example in which functional聽morphogenesis聽of a living system may emerge purely from local interactions at the constituent length scale, thereby providing a source of inspiration for the development of decentralized, autonomous active matter and swarm robotics.
Figures
Top:聽Ant Raft Treadmilling.
Bottom: (A-G) Agent Based Model Schematic.
Citation
Wagner, R. J.; Vernerey, F. J. Computational Exploration of Treadmilling and Protrusion Growth Observed in Fire Ant Rafts. PLoS Comput Biol 2022, 18 (2), e1009869. .