Laboratory for the Physics of Life Thomas Gregor, Professor of Physics, Princeton University

Mircea R. Davidescu, Pavel Romanczuk, Thomas Gregor, Iain D. Cousin. Proc Natl Acad Sci (USA) 120 (11) e2206163120 (2023).

Abstract

How collectives remain coordinated as they grow in size is a fundamental challenge affecting systems ranging from biofilms to governments. This challenge is particularly apparent in multicellular organisms, where coordination among a vast number of cells is vital for coherent animal behavior. However, the earliest multicellular organisms were decentralized, with indeterminate sizes and morphologies, as exemplified by Trichoplax adhaerens, arguably the earliest-diverged and simplest motile animal. We investigated coordination among cells in T. adhaerens by observing the degree of collective order in locomotion across animals of differing sizes and found that larger individuals exhibit increasingly disordered locomotion. We reproduced this effect of size on order through a simulation model of active elastic cellular sheets and demonstrate that this relationship is best recapitulated across all body sizes when the simulation parameters are tuned to a critical point in the parameter space. We quantify the trade-off between increasing size and coordination in a multicellular animal with a decentralized anatomy that shows evidence of criticality and hypothesize as to the implications of this on the evolution hierarchical structures such as nervous systems in larger organisms.

Summary

Coordination between cells is fundamental for multicellular life. The first multicellular animals were capable of growing to indeterminate sizes but lacked nervous systems that could facilitate coordination. We investigate how size variation affects coordination in such organisms by measuring the collective order in the locomotion of Trichoplax adhaerens, the simplest multicellular animal. We find that collective order decreases as such animals grow in size and use a simulation model to determine that this scaling phenomenon occurs at the phase transition between ordered and disordered movement, also known as criticality. Our findings therefore suggest a fundamental trade-off between increasing size and coordination in such a decentralized organism and provide evidence for the necessity of centralized control at larger sizes.