Striated muscles are present in bilaterian animals (e.g. vertebrates, insects, annelids) and some non-bilaterian eumetazoans (i.e. cnidarians and ctenophores). The striking ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin1, 2. Here we show that a muscle protein core set, including a Myosin type II Heavy Chain motor protein characteristic of striated muscles in vertebrates (MyHC-st), was already present in unicellular organisms before the origin of multicellular animals. Furthermore, myhc-st and myhc-non-muscle (myhc-nm) orthologues are expressed differentially in two sponges, compatible with the functional diversification of myhc paralogues before the origin of true muscles and the subsequent deployment of MyHC-st in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess myhc-st orthologues but lack crucial components of bilaterian striated muscles, such as troponin complex and titin genes, suggesting the convergent evolution of striated muscles. Consistently, jellyfish orthologues of a shared set of bilaterian z-disc proteins are not associated with striated muscles, but are instead expressed elsewhere or ubiquitously. The independent evolution of eumetazoan striated muscles through the addition of novel proteins to a pre-existing, ancestral contractile apparatus may serve as a paradigm for the evolution of complex animal cell types.
SUMMARY
Sponges of the species Tethya wilhelma display rhythmic body contractions, which were analyzed by digital timelapse imaging and semi-automated image analysis. For the first time, differential, quantitative data on sponge behaviour could be obtained. The sponges are able to reduce their body volume by up to 73.3% during regular contractions. Each contraction cycle follows a characteristic pattern of four phases, permitting analysis of the kinetics of contraction and expansion. Long-term observations (for >7 days) reveal that the sponge contractions display a day-night periodicity in which contraction cycles are significantly longer during the dark hours. The contractions seem to be mediated by the pinacoderm; they are triggered locally and spread over the sponge surface at 12.5 μm s-1. If two individuals of a clone are fused, the individual contraction rhythm of both sponges persists for several days, until a single new individual sponge is formed with a synchronized rhythm. The reported results and techniques establish T. wilhelma as a model organism for research on the development of aneural signal transduction and integration during early Metazoan evolution.
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