Ciliary flocking and emergent instabilities enable collective agility in a non-neuromuscular animal

Abstract

Effective organismal behavior is characterized by the ability to respond appropriately to changes in the surrounding environment. Attaining this delicate balance of sensitivity and stability is a hallmark of the animal kingdom. By studying the locomotory behavior of a simple animal (Trichoplax adhaerens) without muscles or neurons, here we demonstrate how monociliated epithelial cells work collectively to give rise to an agile non-neuromuscular organism. Via direct visualization of large ciliary arrays, we report the discovery of sub-second ciliary reorientations under a rotational torque that is mediated by collective tissue mechanics and the adhesion of cilia to the underlying substrate.In an illuminating toy model, we show a mapping of this system onto an "active-elastic resonator". This framework explains how perturbations propagate information in this array as linear speed traveling waves in response to mechanical stimulus. Next, we explore the implications of periodic and noisy parametric driving in this active-elastic resonator and show that such driving can excite mechanical 'spikes'. These spikes in collective mode amplitudes are consistent with a system driven by parametric amplification and a saturating nonlinearity. We conduct extensive numerical experiments to corroborate these findings within a polarized active-elastic sheet. These results indicate that periodic and stochastic forcing are critical for increasing the sensitivity of collective ciliary flocking. We support these theoretical predictions via direct experimental observation of linear speed traveling waves which are made possible through the hybridization of spin and overdamped density waves. We map how these ciliary flocking dynamics result in agile motility via coupling between an amplified resonator and a tuning (Goldstone-like) mode of the system. This sets the stage for how activity and elasticity can self-organize into behavior which benefits the organism as a whole.

What is it like to be a choanoflagellate? Sensation, processing and behavior in the closest unicellular relatives of animals

“…Finally, it has been argued that such aggregate behavior is even displayed by some metazoans, for example during ciliary locomotion by the placozoan T. adhaerens, where locomotory ciliated cells of the ventral surface were proposed to all perceive and react to chemoattractants independently (Smith et al 2019). Other studies have, however, put forward evidence of coordination between placozoan cilia (Bull et al 2021).…”

Learning Without Neurons in Physical Systems

“…For example, even in single-celled organisms, we tend to look for a gene regulatory network (or protein interaction circuit) that learns and makes decisions that are then carried out downstream by, say, physical self-assembly or cytoskeletal processes (9). But the downstream "muscle" itself can potentially learn and make decisions, as known to be the case in organisms ranging from ciliates to fruit flies and beehives (10)(11)(12)(13). Physical learning could reveal the broader scope of such nonmodular learning and information processing available for free in the muscle (14).…”

Function and phylogeny support the independent evolution of acid-sensing ion channels in the Placozoa

“…Placozoans similarly exhibit negative locomotory responses to light and gravity (59,90), and positive chemotactic responses to food (algae) and glycine (57,58), as well as start and stop behaviors (56,63,64). A central question is how an animal that lacks body symmetry and a nervous system can generate directed locomotion, especially given that ciliary beating is asynchronous, and that ciliated cells lack overt functional coupling or coordination between them (56,57,91). A model that has been put forward is that individual ciliated cells along the ventral epithelium autonomously detect different concentrations of signaling molecules present along a gradient, generating proportional (graded) responses in altered ciliary beating, such that cells located closer to the ligand source would elicit different responses than those that are farther away.…”