Travelling back in time along the evolutionary tree you eventually reach sponges; possibly the earliest modern animals. Lacking digestive, nervous and muscular systems, it is sometimes difficult to imagine that they are animals, yet sponges could hold the key to the debate about how muscles evolved. Michael Nickel from the Friedrich-Schiller-Universität, Germany, explains that despite lacking muscles, sponges are able to contract, but no one knew how. Competing hypotheses had suggested that either the connective tissue between sponge cell layers – the mesohyl – might mediate the contraction or the outer cell layer – the pinacoderm – could produce squeezing contractions. However, no one had ever tested these ideas and crucially, neither hypothesis could explain how contracted sponges return to their full size. Intrigued by the mystery, Nickel decided to use an X-ray technique to take a close look at contracted and relaxed Tethya wilhelma sponges to find out how they contract without muscles (p. 1692).

First, Nickel made time-lapse movies of a sponge as it contracted and relaxed to see how reproducible the contractions were. Analysing the movies, Nickel could see that each contraction cycle was almost identical. During the first 15 min phase, the relaxed sponge contracted slowly, reducing by 20% of the entire contraction range. But then the contraction accelerated and within 15 mins the sponge had completed the second phase and contracted completely. During the third and fourth phases, the sponge relaxed, expanding by 60% of the entire contraction range over the first 15 min, but then expanded more slowly until returning to its full size 1.25 h after the cycle began.

Next, Nickel looked for differences between the contracted and relaxed sponges with synchrotron radiation-based X-ray microtomography. Teaming up with Jörg Hammel, Nickel dried a contracted and a relaxed sponge ready for transport to Hamburg to use the Deutsches Elektronen Synchrotron to look at the samples with Felix Beckmann. Scanning the sponges with the high intensity X-ray beam, Beckmann and Julia Herzen reconstructed 1–5 μm thick virtual slices through the sponges to produce a 3D view of the sponges and their internal structures.

Looking at the sponge reconstructions, Nickel could see that the volume of the open canals in the relaxed sponge, occupying 72% of the body, had closed down in the contracted sponge to 32%. Also, the mesohyl connective tissue comprised 60% of the contracted sponge's body, as opposed to 28% of the relaxed sponge's body. However, when he compared the absolute volume of the mesohyl in the relaxed and contracted sponges, he could see that it was unchanged. The mesohyl was not involved in the contraction phase of the sponge's cycle. Then, Nickel measured the volume of the thin outer pinacoderm layer relative to the mesohyl volume, and he found that the volume of the pinacoderm layer had reduced 2.75-fold. The pinacoderm was driving the sponge's contraction.

Having confirmed that the pinacoderm is responsible for sponge contraction, Nickel says, ‘I was surprised how clearly our results support one of the two hypotheses,’ and adds, ‘This leads to the question of whether epithelial contractility is a character in the ground pattern of the Metazoa. I think it is an interesting hypothesis and will fuel the discussion on the evolutionary transition from non-muscular contractile cells to muscle cells.’ Also, he does not rule out a role for the mesohyl in the sponge's contraction cycle, suggesting that spindle-shaped cells in the mesohyl could behave as antagonists to the pinacoderm's contraction and return contracted sponges to their full size.

J. U.
The contractile sponge epithelium sensu lato – body contraction of the demosponge Tethya wilhelma is mediated by the pinacoderm
J. Exp. Biol.