Evolution of body contractility in early branching Metazoa – what morphology of Porifera and Placozoa tells us

Early muscle cell evolution has been discussed for over acentury. However, the emergence of contractile muscle filamentsis still an unresolved mystery. The Cnidaria posses thefirst muscle cells among the Metazoa, while the Porifera andPlacozoa are muscleless. Nevertheless, both display a remarkablerange of body contractility, but the effector cells are stilldebated. Two competing hypotheses on sponge contractilecells were postulated: (1) mesohyl contraction actinocytes(“myocytes”). (2) epidermal contraction by pinacocytes. In thePlacozoa, the mesenchymal fibre cells are regarded contractile.Only indirect evidence, like cell shape or the presence ofcytoplasmic filaments supports contractility of those cells. Wepresent comprehensive data on sponge contractility includingall four major sponge taxa, Demospongiae, Hexactinellida,Calcarea and Homoscleromorpha. In addition, the contractilebehavior of Trichoplax adhaerens is addressed. A modernfunctional morphology approach based on in vivo and 3D imagingtechniques (i.e. SRµCT), provides evidence for epithelialcontractility. In conclusion, epithelial contractility might be acharacter of the metazoan ground pattern. Most likely suchearly contractile epithelia lacked functional compartmentalizationlike in cnidarian epithelio-muscle cells. The resulting evolutionaryscenario suggests that the transition from a generalcytoskeleton contractility (also found in unicellular membersof the Opistokonta) to the muscle specific, specialized filamentcontractility, occurred early within the metazoan stem group.The contractile epithelia in Porifera and Placozoa might bothbe derived, but nevertheless share a functional root on the geneand protein level. This hypothesis will have to be tested usinggenomic data and gene expression analysis