Abstract
Effective organismal behavior responds 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 (\textit{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 a
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 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 valuable
for increasing the sensitivity of collective ciliary flocking. We support these
theoretical predictions via direct experimental observation of linear speed
traveling waves which arise from 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.