Abstract

Compared to other forms of multicellularity, the animal case is unique. Animals—barring some exceptions—consist of collections of cells that are connected and integrated to such an extent that these collectives act as unitary, large free-moving entities capable of sensing macroscopic properties and events. This animal configuration is so well-known that it is often taken as a natural one that ‘must’ have evolved, given environmental conditions that make large free-moving units ‘obviously’ adaptive. Here we question the seemingly evolutionary inevitableness of animals and introduce a thesis of bodily complexity: The multicellular organization characteristic for typical animals requires the integration of a multitude of intrinsic bodily features between its sensorimotor, physiological, and developmental aspects, and the related contraction-based tissue- and cellular-level events and processes. The evolutionary road toward this bodily complexity involves, we argue, various intermediate organizational steps that accompany and support the wider transition from cilia-based to contraction/muscle-based motility, and which remain insufficiently acknowledged. Here, we stress the crucial and specific role played by muscle-based and myoepithelial tissue contraction—acting as a physical platform for organizing both the multicellular transmission of mechanical forces and multicellular signaling—as key foundation of animal motility, sensing and maintenance, and development. We illustrate and discuss these bodily features in the context of the four basal animal phyla—Porifera, Ctenophores, Placozoans, and Cnidarians—that split off before the bilaterians, a supergroup that incorporates all complex animals.

Highlights

  • Multicellular systems evolved from unicellular ancestors on at least 25 independent occasions, both in prokaryotes and eukaryotes (Bonner, 2000)

  • Ctenophores express a diversity of innexins, and opsins necessary for a sensory neuron for photo-reception (Jekely et al, 2015). All these findings suggest the existence of a complex peptidergic armory in the Ctenophores nervous system that, to the Cnidaria regulate the animal’s physiology

  • Apart from the feeding-related cells in Cnidaria and Ctenophora we find distinct cells related to the sensorimotor behavior of the animal such as myoepithelial cells or pure muscle cells, nerve cells and several sensory cells

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Summary

Introduction

Multicellular systems evolved from unicellular ancestors on at least 25 independent occasions, both in prokaryotes and eukaryotes (Bonner, 2000). Of these 25 occasions, six eukaryote lineages gave rise to complex multicellularity. Complex multicellularity arose once within the animal (metazoan) lineage (e.g., Bonner, 1988; Medina et al, 2003; Knoll, 2011). Based on previous work (Arnellos and Moreno, 2016; Keijzer and Arnellos, 2017), our goal in this paper is to further discuss and argue on the special organizational characteristics and the related bodily complexity necessary for the evolution of animal multicellularity

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