Dynamics and emergence of metachronal waves in the ciliary band of a metazoan larva

Both natural and synthetic ciliary arrays exhibit diverse coordination patterns. Proper coordination of cilia is essential for the normal physiology of many organisms, from single cells to humans. Yet despite decades of research the mechanisms of cilia coordination remains disputed, particularly the question of how coordinated waves of activity known as metachronal waves arise in different ciliated systems. In many aquatic larvae that rely on ciliary motility to swim, the cilia are often arranged ornately in arrays or bands, within which robust metachronal waves propagate. Here, to resolve the origins of ciliary metachronism, we target the equatorial ciliary band of the marine annelid, Platynereis dumerelii , using whole-body high-speed imaging, and physical and biological manipulations. The results reveal an unprecedented wave structure featuring strong coupling within individual multiciliated cells that breaks down across cell boundaries, and absence of global coupling across the organism. Using laser ablation to create gaps in the ciliary band, we quantify the resulting disruption to wave propagation, revealing the extent of interciliary phase-locking and implicating steric interactions as an important contributor to coordination. The larvae also exhibit spontaneous whole-body ciliary arrests which allow us to study wave emergence and re-establishment for the first time, revealing a novel role of the animal’s nervous system in the dynamic coupling of cilia.