Animals, amoebae and assumptions

Animals aren’t the only multicellular creatures in their phylogenetic neighbourhood. Social amoebae, many fungi and quite a few of the poorly known choanoflagellates spend at least part of their lives as collections of cooperating cells. Conventional wisdom has been that these groups invented multicellularity independently, but maybe conventional wisdom needs a bit of challenging.

To tell you the truth, I never really thought about the other possibility, that being multicellular is the original state of affair for these organisms. I never really considered the evidence on which the conventional wisdom was based. You could say I didn’t really care either way. A while back I saw a paper that said something about a social amoeba having an epithelium, but I just kind of shrugged and went on with my life. I don’t know, now an article in BioEssays brought this up again, and I’m not sure I was right to ignore it back then. I think Dickinson et al. (2012) have a point, and I think some assumptions may need to be reexamined.

In case you wondered, an epithelium is a type of tissue made of a layer or layers of polarised cells. “Polarised” means that various cellular components – proteins, attachments to neighbouring cells, organelles – are distributed unevenly in the cell, clustered towards one or the other side of the cell layer. Epithelia line pretty much everything in a typical animal’s body, from, well, the entire body, to things like guts and glands. They secrete important stuff like hormones, and their closely packed cells form a barrier to keep molecules and pathogens where they belong. An epithelium was thought to be a uniquely animal thing to have, but looking more closely at that weird little amoeba suggested it may not be.

The paper that I ignored was Dickinson et al. (2011) – yes, by the exact same people who wrote the BioEssays piece. OK, I didn’t completely ignore it. I read enough of it to scribble a quick note in my citation manager saying “screams convergent evolution to me”. The paper examined the multicellular stage in the life of Dictyostelium discoideum, an ordinarily single-celled amoeba that reacts to food shortages by crowding together with friends and family to form a fruiting body that helps disperse some of its cells in search of new habitats. The fruiting body is pretty complex for a “unicellular” creature, and it turns out that this complexity includes a region of tissue that looks quite a lot like a simple epithelium. It doesn’t just look like one; it sorts out its insides and outsides with the help of proteins called catenins, which are also involved in cell polarity in the epithelia of animals. (Below: D. discoideum being multicellular, from Wikipedia)

That isn’t much evidence to base an inference of homology on, especially since other key players in animal cell polarity are entirely absent from D. discoideum. But equally, the fact that tons of unikonts (the group including amoebae, slime moulds, fungi, choanoflagellates and animals) are single-celled doesn’t mean that the multicellular groups all came up with the idea independently. Evolution doesn’t always increase complexity – sometimes complexity becomes superfluous.

I remember when we discussed the choanoflagellate genome paper (King et al., 2008) in class. The genome in question belongs to a purportedly single-celled creature, but it contains tons of genes you’d think only multicellular organisms would need, such as genes for cell-to-cell adhesion proteins. So one explanation is that these proteins originally did something else, like anchoring a single cell to its favourite spot. Another explanation is that they did have something to do with multicellularity – it just wasn’t the multicellularity of animals at first.

This suggestion isn’t terribly controversial when you’re talking about choanoflagellates, since some of them do obviously form colonies (one such colony of Salpingoeca/Proterospongia rosetta is shown below, from Mark Dayel of the King lab via ChoanoWiki). It’s not hard to imagine that either the “single-celled” species whose genome was sequenced also has a colonial stage the scientists just never saw, or that its recent ancestors did.

Whether or not the same applies to the whole of unikonts is a more difficult question. I’m not at all familiar with the details of unikont relationships, but based on the tree shown in the BioEssays article, multicellularity is all over the group. In most cases, it’s facultative multicellularity; animals are rather the exception in being doomed to it for their entire lives. However, if you just looked at that tree, you’d wonder why the hell anyone thought the common ancestor of these things wasn’t some kind of multicellular.

Yet the details of animal-like multicellularity aren’t so widespread. True cadherins (the cell adhesion proteins I mentioned) have only been found in animals proper. Choanoflagellates and some even more obscure relatives of animals have bits and pieces of them, and other unikonts have none at all as far as anyone knows. Epithelium-like tissues have only been described in that one species of amoeba – but, as Dickinson and colleagues note, no one really looked in the others.

Personally, I wouldn’t be at all surprised if the conventional wisdom ended up shifting. I still don’t think that the evidence from Dictyostelium is enough to draw a conclusion. We obviously need to know a lot more about unikont genomes, tissues and life cycles to piece together the history of multicellularity in the group, but I’m not sure that right now a unicellular ancestor has a lot more going in its favour than a multicellular one. Guess we’ll have to wait and look with an open mind 🙂

***

References

Dickinson DJ et al. (2011) A polarized epithelium organized by β- and α-catenin predates cadherin and metazoan origins. Science 331:1336-1339

Dickinson DJ et al. (2012) An epithelial tissue in Dictyostelium challenges the traditional origin of metazoan multicellularity. BioEssays advance online publication, 29/08/2012, doi:10.1002/bies.201100187

King N et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783-788

 

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