Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses

Abstract

Trichoplax adhaerens is a flat, millimeter-sized marine animal that adheres to surfaces and grazes on algae. Trichoplax displays a repertoire of different feeding behaviors despite the apparent absence of a true nervous system with electrical or chemical synapses. It glides along surfaces to find food, propelled by beating cilia on cells at its ventral surface, and pauses during feeding by arresting ciliary beating. We found that when endomorphin-like peptides are applied to an animal, ciliary beating is arrested, mimicking natural feeding pauses. Antibodies against these neuropeptides label cells that express the neurosecretory proteins and voltage-gated calcium channels implicated in regulated secretion. These cells are embedded in the ventral epithelium, where they comprise only 4% of the total, and are concentrated around the edge of the animal. Each bears a cilium likely to be chemosensory and used to detect algae. Trichoplax pausing during feeding or spontaneously in the absence of food often induce their neighbors to pause as well, even neighbors not in direct contact. Pausing behavior propagates from animal to animal across distances much greater than the signal that diffuses from just one animal, so we presume that the peptides secreted from one animal elicit secretion from nearby animals. Signal amplification by peptide-induced peptide secretion explains how a small number of sensory secretory cells lacking processes and synapses can evoke a wave of peptide secretion across the entire animal to globally arrest ciliary beating and allow pausing during feeding.

The radial expression of dorsal-ventral patterning genes in placozoans,Trichoplax adhaerens,argues for an oral-aboral axis

“…In Hydrozoan cnidarians, the nervous system is thought to be derived from I-cells that orginate in the endomesoderm (gastroderm) during embryonic development [89][90][91], although sensory cells can emerge from I-cell free animals [92,93]. In the absence of a true nervous (or musculature) system, neuropeptide and calcium signaling play a role in complex behaviors of these animals [94,95]. Our findings, although suggestive, require greater analysis and further study to truly understand how these and other developmental genes shape the body of Trichoplax.…”

High cell diversity and complex peptidergic signalling underlie placozoan behaviour

“…An earlier study reports that gland cells secrete an endomorphin-like peptide, which arrest ciliary beating, inducing feeding-like pauses [24] ( Figure S5). Interestingly, we observed that the application of the endomorphin-like peptide also induced flattening but no churning (Table S1).…”

“…Only individuals that were visible during the entire time of the recording were tracked. Since animals in close contact may coordinate their behaviours [17,24], only animals which were not in contact with one another were monitored to avoid oversampling. In rare cases when individuals were in contact with each other, only one was monitored.…”

“…In addition, SIFGamide-treated animals often partially detached from the substrate (Figure 2E, G-H; Movie S2). Detachment was briefly reported elsewhere [24]. These effects are reminiscent of the shape T. adhaerens adopts in response to UV light [25] or when flushed with a strong water stream.…”

Placozoa and Cnidaria are sister taxa

“…The discovery 1 and mid-20 th century rediscovery 2 of the enigmatic, amoeba-like placozoan Trichoplax adhaerens did much to ignite the imagination of zoologists interested in early animal evolution 3 . As 48 microscopic animals adapted to extracellular grazing on the biofilms over which they creep 4 , placozoans have a simple anatomy suited to exploit passive diffusion for many physiological needs, with only six morphological cell types discernible even to intensive scrutiny 5,6 , and have no conventional muscular, digestive, or nervous systems, yet show tightly-coordinated behavior 7,8 . They 52 proliferate through fission and somatic growth.…”