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Xenoturbella is an odd little organism. We can't say that it has a face only a mother could love, because it doesn't have a face. Or a brain. Or appendages. Or even a through gut, just a blind cul-de-sac. Xenoturbella is a completely unassuming little blob that seems to want nothing more in life than to wallow in the mud of the North Sea. For systematists, its extreme simplicity and hence shortage of obvious with any other taxa have made it into something of a nuisance. Generally it has been lumped with the , which also lack a through gut. Nevertheless, differences in anatomical structure of most organs made this a very uneasy arrangement. Haszprunar et al. (1991). So Xenoturbella was for the most part effectively swept under the rug until 1997, when two studies announced that it was a . Gee (2003); Bourlat et al. (2003). Not only did molecular analysis place it among , but bivalve eggs and larvae were found within specimens. It was thus inferred that Xenoturbella began life as a typical bivalve, but over the course of development all features indicative of its origin were lost. The problem was that such a total obliteration was in stark contrast to the apparent normality of the molecular data. Indeed, the Xenoturbella sequences actually nested within the genus , a basal but fairly unremarkable bivalve - the SSU rDNA sequence was identical to that of .

In 2003, Bourlat and co-workers gave an explanation for this paradox -- the sequences came not from Xenoturbella, but from Nucula larvae that it had ingested. Xenoturbella is not a mollusc, but a . Bourlat et al. identified another sequence that appeared to come directly from Xenoturbella, as shown by its amplification from specimens with the gut removed. These sequences grouped with the , specifically with the . Unlike the mollusc hypothesis, this result was not entirely novel. Reisinger had suggested in 1960 that Xenoturbella might be derived from a deuterostome larva based on features of the nervous system, the -like and the . Haszprunar et al. (1991). Bourlat et al. suggested a position as the sister group of Ambulacraria to be more likely than one within it due to usage. For instance, the ATA codon codes for as in most , rather than as in Ambulacraria.

The characters shared by Ambulacraria and suggest that Xenoturbella is secondarily simplified, rather than representing the ancestral form for deuterostomes. Such secondary simplification is unusual in a free-living organism. It is more common in parasitic forms. How Xenoturbella managed to lose many of the features its ancestors undoubtedly had is completely unknown.

© Christopher Taylor, CKT050827.

Additional note: Christopher Taylor's discussion of Xenoturbella was sufficiently intriguing that we decided to poke around a bit further. One further objection to ambulacrarian status for Xenoturbella comes from the embryological work of Israelsson (1999). Israelsson, working with rare and difficult material, it should be noted, found that embryos associated with Xenoturbella were of a perfectly normal type. This is exactly what one might expect of mollusks in general, and of Nucula in particular. However, specimens undergoing transformation at several months of age apparently lose all of the complexity and internal organization which they developed as embryos. Israelsson was not able to obtain free-living larvae at some intermediate stage. However, judging from the embryo, they would be indistinguishable from other molluscan larvae. This data, Israelsson argues, clearly shows that Xenoturbella is a degenerate mollusk. However, it also makes it quite difficult to explain why Xenoturbella develops all these molluscan bells and whistles in the first place.

Israelsson's remarks suggested that it might be a good idea to look harder at his images. As shown above in red, there is a curious, unlabelled mass associated with the . With not too much imagination, it could be mistaken for a smaller version of the late-stage Xenoturbella larva on the right of the image, also from Israelsson (1999). The two images are almost exactly to scale, with scale bar = 500µ in both.

A close reading of the paper suggests two alternate possibilities. First, this mass might be an early manifestation of the . However, if we correctly interpret Israelsson's figures, the unlabelled mass is located almost directly opposite from the foot muscle at this stage of development. Second, the unlabelled mass might be the (gill). Its relationship with the presumed pleural ganglion is about right. However, it looks nothing like Israelsson's line drawing of the ctenidium. (Just for fun, we have also pointed out the slight resemblance between this structure and the stage of [Echinodermata] development. Although not visible in the photograph, the auricularia also has ciliated bands like the ctenidium.)

So where does this leave us? Granted, this is all a bit of a shot in the dark, but there is a third possibility. Perhaps the unlabelled mass is actually the early developmental stage of Xenoturbella, while the rest is -- just as it appears -- an embryo of Nucula. That is, perhaps Xenoturbella develops as an of Nucula embryos. In that case, we would suppose that Xenoturbella injects its own eggs inside the growing embryos of Nucula. The Xenoturbella embryo then consumes the Nucula embryo from within. It emerges into the environment as a very simple planktonic worm, feeds (not necessarilly on Nucula) and grows. Eventually, it captures more Nucula embryos of its own, and continues the cycle.

This hypothesis explains much that is otherwise obscure. For example, Xenoturbella looks like a highly simplified parasitic form because, developmentally, it is a highly simplified parasitic form. The non-parasitic adult form is only a bridge between parasitic developmental forms. Free embryonic forms of Xenoturbella are never found because no such embryos exist except inside Nucula embryos. Similarly, larval forms of Xenoturbella are never found because development is direct. Fertile eggs of Nucula are routinely found in the gut of adult Xenoturbella for the very good reason that Xenoturbella cannot reproduce without them. We might conclude, then, that Xenoturbella is neither mollusk nor molluscivore, but an obligate developmental parasite of bivalves. ATW050828.

Christopher adds: Another possibility to explain the simplicity of Xenoturbella that might be more likely (though really equally hypothetical) is that it has gone through a size squeeze at some point in its ancestry. In other words, at some point an ancestral deuterostome became really small, probably as a member of the , and lost a number of complicated organ systems as a result. Compare what happened to the among the (loss of , heart, and ; body form strongly simplified, with very short life cycle). Xenoturbella then once again became bigger, but with a simplified organ system. However, short of actually finding micro-xenoturbellids, it would be very difficult to test this idea. CKT050901.

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