Salinella - what the crap was it?

In 1991, Haszprunar et al. published a brief book chapter in which they listed a collection of modern animals of exceedingly uncertain relationships. Any one of those organisms would make for an interesting blog - some of them have now been placed with reasonable confidence in the animal family tree. The worm-like Xenoturbella masqueraded as a mollusc for a while, but now appears to be a basal deuterostome (Bourlat et al., 2003 - see Palaeos.com for a section I wrote on this affair a couple of years ago). The also-worm-like Buddenbrockia has, rather spectacularly, been shown to be a very basal member of the parasitic Myxozoa, the least animal-like of all animals (Okamura et al., 2002). But today, I'm going to touch on perhaps the most mysterious of all Haszprunar et al.'s subjects - Salinella salve Frenzel 1892.

Salinella has only ever been found once, in a saline culture derived from salt beds in Argentina (Brusca & Brusca, 2003 - see Answers.com for further details). It was described as having a unique body plan, with a single layer of cells surrounding a hollow sac, open at both ends. All cells were densely covered by cilia both inside and out, and there were longer cilia around the openings (which were the mouth and anus). Other than that, there appears to have been no distinction into organs, tissues, whatever. Salinella moved by ciliary gliding, and reproduced asexually by fission.

If this description was accurate, then the affinities of Salinella become very difficult indeed. The presence of a through-gut of sorts gives Salinella a superficially bilaterian appearance, but there is no way it could be a bilaterian. All known bilaterians are triploblastic (i.e. possess three basic cell layers, with the possible exception of mesozoans, if they are reduced bilaterians), and even the outgroup of bilaterians, whether cnidarians or ctenophores, has at least a diploblastic organisation (two cell layers). Even sponges are essentially diploblastic. If there was a monoblastic stage in the evolution of animals, as has been suggested by some authors, then it would have been very early in their history. It is possible that Salinella might represent this stage, which has inferred from the blastula stage in embryonic development (Clark, 1922).

Salinella has been compared in the past to the simple animals Trichoplax and the Mesozoa. Trichoplax (generally placed in its own phylum, Placozoa) is a flattened organism with only four cell types, and has been referred to as the simplest-organised animal known (Syed & Schierwater, 2002). It basically comprises an upper epithelium, a lower epithelium and a central mass of cells. Digestion occurs through the formation of a hollow underneath the lower epithelium into which the animal exudes digestive juices and absorbs nutrients. Epithelial cells are ciliated, but externally only.

The Mesozoa are two groups of internal parasitic animals, the Orthonectida and Dicyemida (it is now thought quite likely that these two groups are not closely related to each other). Both have a basic structure of an outer layer of ciliated cells surrounding a central mass. In dicyemids, the central sector is a single long tube cell. In Orthonectida, the central area contains gametes. Before the formation of gametes, orthonectids are a multinucleate plasmodium without distinct cells.

Beyond the superficial similarity of undifferentiated cell layers, however, Salinella as little in common with these animals. It has long been suggested that, rather than being primitively simple organisms, mesozoans represent derived animals that have become secondarily simplified as a result of their parasitic lifestyles. For both groups, there is genetic evidence to support this (Hanelt et al., 1996; Kobayashi et al., 1999). Trichoplax has a better claim to be genuinely primitive. However, Salinella lacks Trichoplax's central cellular layer, and Trichoplax does not have Salinella's cilia on both sides of the cell. And certainly there is no similarity between Trichoplax's external digestion and Salinella's through gut.

Which brings us to the final possibility, the one that many zoologists have suspected - Salinella never actually existed. It is possible that Frenzel was mistaken in his description of Salinella's structure (I've never seen Frenzel's original description, and I'd be interested in seeing how likely this is). Could Frenzel have actually been looking at Trichoplax-like organism? Unfortunately, unless more specimens of Salinella are recovered, we are unlikely to ever know. And if Frenzel was severely mistaken, then even if the organism he was looking at is recovered, it may never be recognised as such.

REFERENCES

Bourlat, S. J., C. Nielsen, A. E. Lockyer, D. T. J. Littlewood & M. J. Telford. 2003. Xenoturbella is a deuterostome that eats molluscs. Nature 424: 925-928.

Brusca, R. C., & G. J. Brusca. 2003. Invertebrates, 2nd ed. Sinauer Associates, Inc., Publishers: Sunderland (Massachusetts).

Clark, A. H. 1922. Animal evolution. Proceedings of the National Academy of Sciences of the USA 8: 219-225.

Hanelt, B., D. Van Schyndel, C. M. Adema, L. A. Lewis & E. S. Loker. 1996. The phylogenetic position of Rhopalura ophiocomae (Orthonectida) based on 18S ribosomal DNA sequence analysis. Molecular Biology and Evolution 13 (9): 1187-1191.

Haszprunar, G., R. M. Rieger & P. Schuchert. 1991. Extant "problematica" within or near the Metazoa. In The Early Evolution of Metazoa and the Significance of Problematic Taxa (A. M. Simonetta & S. Conway Morris, eds.) pp. 99-105. Cambridge University Press.

Kobayashi, M., H. Furuya & P. W. H. Holland. 1999. Dicyemids are higher animals. Nature 401: 762.

Okamura, B., A. Curry, T. S. Wood & E. U. Canning. 2002. Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilaterian origin of the Myxozoa. Parasitology 124: 215-223.

Syed, T., & B. Schierwater. 2002. Trichoplax adhaerens: discovered as a missing link, forgotten as a hydrozoan, re-discovered as a key to metazoan evolution. Vie Milieu 52 (4): 177-187.