Petrified strawberries and the cnidarian that isn’t

In the last few weeks, tons of squee-worthy stuff has accumulated on my backlog. The echinoderm transitional form from Cambrian Morocco I got so excited about is now officially described (Smith and Zamora, 2013), Dennis Duboule and his team put out some really cool findings about how vertebrate Hox clusters work that connect to my old fascination with limb evo-devo (Andrey et al., 2013), the developmental hourglass returned (Schep and Adryan, 2013)…

I kind of regret not gushing about all of them, but let’s face it, I’m not gonna ever do that. Looking over the things I bookmarked recently, I decided I’d rather not ignore Yasui et al. (2013), though. One, it’s about early animals, two, it exploits one of the greatest treasures the fossil record has to offer: the record of ancient development. I almost don’t care what the findings are, because the fact that we can follow a 530+-million-year-old creature from egg to adult is so staggeringly awesome in itself that everything else pales in comparison.

The paper looks at a tiny creature known from the earliest Cambrian of China. The beastie is called Punctatus and looks something like this (the authors’ interpretation of its development from fig. 4 of the paper):

The observations in this paper come from some 10 thousand specimens of various developmental stages from a couple of different Punctatus species. With such an abundance of fossils covering the animal’s life cycle, it is possible to connect the different stages and identify them as the same animal. So how did Punctatus develop and what kind of animal was it?

The earliest development took place inside a smooth egg membrane. Broken or CT-scanned embryos show that the creatures went through a nice blastula stage that looked like a simple, hollow ball of cells which were maybe a bit fatter on one side than the other (below, left). This type of blastula is quite common, found in animals as disparate as jellyfish (middle, from celldynamics.org) and sea urchins (right, from exploratorium). So the blastulae don’t tell you much about the affinities of the creature. In fact, while the authors use the leftmost embryo as a pretty illustration, they’re not even sure this particular specimen belongs to Punctatus. (Which is not really surprising.)

coeloblastulae

By the time young Punctatus hatch from their eggs, they are much more identifiable. The authors compare them to strawberries (awwww! ^.^). They are spiny all over, slightly pointy on one end and slightly flattened on the other, and the flattened end is divided into five parts by a star-like pattern of Y-shaped grooves. At the centre of the star, there is the blastopore, the opening of the embryonic gut, which seems to develop straight into the mouth in this creature. Punctatus never develops another gut opening. The simple blastopore = mouth equation again isn’t terribly informative, since a lot of animals follow it, and it’s the most straightforward way to make a mouth. The only thing the lack of a through gut tells us is something that was already fairly obvious – Punctatus is not a bilaterian.

The early stages also exclude another group from the list of possible identities, that is ctenophores. Early embryos of modern ctenophores (comb jellies/sea gooseberries) have very unequal-sized cells (see image at the top of this article), and no such embryos are known from the deposits preserving Punctatus specimens. (Although given what I recently learned about living ctenophores having a very recent common ancestor, I wouldn’t bet on what their Cambrian ancestors were up to…)

Thirdly, embryos that haven’t yet hatched also tell us something important about the adults. The prickly covering of these animals had apparently been interpreted as the remnants of a tube in which the animal proper lived – but this covering clearly appears before the baby even pops out of the egg, and the mouth forms right in the middle of it. All of that makes it more likely to be the animal’s skin. And that weakens a possible link to a group of extinct tube-dwelling animals that are much more plausibly related to jellyfish.

After hatching, development enters a new stage. In young and adult Punctatus specimens, the strawberry-like hatchling body remains in place, but a new body region appears at the mouth end, which has a ringed appearance and no spines. Presumably, individuals with more rings were older.

CT cross-sections of such specimens (C-E below) show a huge, empty body cavity, with a small sac-like gut attached to the mouth. There’s apparently no “stuff” between the gut and the body wall: no mesenteries anchoring the gut, no jelly or mass of cells filling in the body cavity, just big fat nothing. This is unlike not just bilaterians or ctenophores, but also cnidarians, in which the gut wall tends to be much closer to the body wall, and a jelly-like layer containing a varying amount of cells fills any gaps between the two.

From this point, the basic body plan doesn’t seem to change. Specimens with only a couple of rings and those with a dozen have the same small gut and large body cavity. There’s nothing we might call metamorphosis – unlike most cnidarians, Punctatus didn’t have a larval stage. (BTW, can someone tell me what the hell the lumpy bit on top of G above is? The paper doesn’t bother to explain as far as I could tell, and it bugs me.)

An intriguing (and rather pretty) part of the animal is the mouth end, what the authors call the “oral ruffle”. You’ll see why it’s called that if you look at figure 3:

This is an inferred developmental series of the mouth region. The five-pointed star of the hatchlings develops into ten finely striped folds emerging from the body surface, and as the animal grows, a new oral ruffle appears inside the previous one. The old ruffle then becomes part of the body wall, forming the next ring. Rinse and repeat. There are no tentacles at any point, although this might still turn out to be an artefact of preservation.

Tenfold symmetry, stacks old oral ruffles, no tentacles, building an adult body on top of an intact piece of embryo – the whole thing is quite unlike your typical cnidarian. Or, indeed, your typical anything else. The authors use the unusual developmental and body plan features of this creature to question its previous assignment to cnidarians, but beyond that, they are unsure what to make of it.

Well, this is the Early Cambrian, when a lot of now-extinct animal lineages were kicking around. Of course they would give us classification headaches! 😉 Which probably means that we know an awful lot about the development of a member of a long-extinct lineage. That’s a comparative embryology goldmine right there, folks!

***

References:

Andrey G et al. (2013) A switch between topological domains underlies HoxD genes colinearity in mouse limbs. Science 340:1234167, doi:10.1126/science.1234167

Schep AN, Adryan B (2013) A comparative analysis of transcription factor expression during metazoan embryonic development. PLoS ONE 8:e66826

Smith AB, Zamora S (2013) Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan. Proceedings of the Royal Society B advance online publication 26/06/2013, doi:10.1098/rspb.2013.1197

Yasui K et al. (2013) A diploblastic radiate animal at the dawn of cambrian diversification with a simple body plan: distinct from Cnidaria? PLoS ONE 8: e65890

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