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Curr Biol. 2018 Nov 5;28(21):3495-3501.e2. doi: 10.1016/j.cub.2018.08.067. Epub 2018 Oct 18.

High Cell Diversity and Complex Peptidergic Signaling Underlie Placozoan Behavior.

Author information

1
Department of Fundamental Neurosciences, University of Lausanne, Rue du Bugnon 9, 1005 Lausanne, Switzerland.
2
Living Systems Institute, University of Exeter, Stocker Road, EX44QD Exeter, UK.
3
ITZ, Ecology and Evolution TiHo Hannover, Bünteweg 17d, 30559 Hannover, Germany.
4
Living Systems Institute, University of Exeter, Stocker Road, EX44QD Exeter, UK. Electronic address: g.jekely@exeter.ac.uk.
5
Department of Fundamental Neurosciences, University of Lausanne, Rue du Bugnon 9, 1005 Lausanne, Switzerland. Electronic address: dirk.fasshauer@unil.ch.

Abstract

Placozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioral control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive cells for communication during the rise of animals are not yet understood [1-5]. The placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple body plan [6-9]: a thin upper epithelium and a columnar lower epithelium interspersed with a loose layer of fiber cells in between. Its genome contains genes encoding several neuropeptide-precursor-like proteins and orthologs of proteins involved in neurosecretion in animals with a nervous system [10-12]. Here we investigate peptidergic signaling in T. adhaerens. We found specific expression of several neuropeptide-like molecules in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected cell-type diversity of T. adhaerens. Using live imaging, we discovered that treatments with 11 different peptides elicited striking and consistent effects on the animals' shape, patterns of movement, and velocity that we categorized under three main types: (1) crinkling, (2) turning, and (3) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signaling in nerveless placozoans and suggest that peptidergic volume signaling may have pre-dated synaptic signaling in the evolution of nervous systems.

KEYWORDS:

Trichoplax adhaerens; animal evolution; cnidarians; ctenophores; early metazoans; nervous system evolution; peptidergic signaling; placozoans; porifera

PMID:
30344118
DOI:
10.1016/j.cub.2018.08.067
[Indexed for MEDLINE]
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