Thursday, May 14, 2009

Searching for the Urbilaterian

The early origins of the animal phyla contain many intriguing mysteries. It's generally accepted today that the sponges represent the earliest form of multicellular animals, sharing with the choanoflagellates the central flagellum surrounded by a collar of microvilli which are connected by a thin membrane that both use as for feeding. (An intriguing recent study9 suggests that the placozoa, an extremely simple (or simplified) non-parasitic animal, is actually the sister group of the sponges (including eumetazoa), branching earlier than the divisions within the sponges but later than the choanoflagellates.)

Figure 1: free-swimming choanoflagellate. (From Wiki.)

One group of the sponges, the Calcareous sponges, developed a lineage that evolved into all the other forms of animal life we're used to, called the Eumetazoans (for "good" or "well formed" metazoans). Today, these may be generally grouped into the Ctenophores (or "comb jellies"), the Cnidaria, and the Bilateria, which (in theory) comprise all animals with bilateral symmetry.

It's at the root of the Bilateria that our current mystery exists. One of the simplest type of bilaterian, called the Acoela, has often been regarded as typical of this ancestor,2, 3, 6, 7, 8 based primarily on molecular evidence. Now, a just published study, To Be or Not to Be a Flatworm: The Acoel Controversy (by Bernhard Egger, Dirk Steinke, Hiroshi Tarui, Katrien De Mulder, Detlev Arendt, Gaƫtan Borgonie, Noriko Funayama, Robert Gschwentner, Volker Hartenstein, Bert Hobmayer, Matthew Hooge, Martina Hrouda, Sachiko Ishida, Chiyoko Kobayashi, Georg Kuales, Osamu Nishimura, Daniela Pfister, Reinhard Rieger, Willi Salvenmoser, Julian Smith, Ulrich Technau, Seth Tyler, Kiyokazu Agata, Walter Salzburger, and Peter Ladurner) further complicates the matter by finding a pair of important characteristics that this group shares with some more complex animals, the Rhabditophora, a major subgroup of Platyhelminthes, the flatworms.

Ever since the onset of cladistics, Platyhelminthes has been the subject of controversy over its position in the animal tree of life. Originally, the Acoela and another group called the Nemertodermatida were placed in Platyhelminthes based on morphological similarities. But virtually all molecular studies place them basal to the bilaterians: that is they represent the earliest branch of the bilaterian tree. At the same time, the remainder of Platyhelminthes is placed by molecular studies well within the Lophotrochozoa (see the relationship chart here).

This paper documents that the acoels share two similarities with the Rhabditophora:

1. A unique distribution and proliferation of stem cells and specific mode of epidermal replacement, and

2. The expression of certain microRNA genes in a place no other known animal expresses them.

There are three ways to explain this:

Alternative 1: The stem-cell system is a synapomorphy of Acoela and Rhabditophora

That is, it's an innovation that they share from a recent common ancestor.

Alternative 2: The stem-cell system of Acoela and Rhabditophora is a plesiomorphy

That is, they share it from the common ancestor of all bilaterials.

Alternative 3: The stem-cell system of Acoela and Rhabditophora is a product of convergent evolution

That is, they evolved it separately.

Alternative 1 would seem to be most parsimonious, except that it flatly contradicts just about every molecular study of the situation, as well as certain other studies based on morphology.

What does that mean? Basically, the whole issue is back up in the air:
It appears that until substantial sampling of lower taxa among flatworms is performed, and more studies on stem cells in non-rhabditophoran flatworms are available, none of the competing phylogenetic hypotheses can be favored.

What are the implications? Are we ever going to know, or even have a single strong theory, what the "ubilaterian", the original common ancestor of all bilaterians, was like?

Let's take it a little further than just analyzing the characteristics of the various phyla. In a recent post I mentioned the need to ask just how each species (presumably ancestral to a phylum) came to evolve. I'm going to do a little speculating here.

Coelom Considerations

To begin with, let's take a look at the coelom. Wiki defines it as "fluid filled cavity formed within the mesoderm." It goes on to say, "Coeloms developed in triploblasts but were subsequently lost in several lineages." This is an example of how the Kuhnian Paradigm works. An assumption like this gets "built in" to all the questions and research people do, and tends to distort the entire research process. Perhaps they didn't. Perhaps coeloms developed independently in a number of lineages after the acoela had already branched off. How much does it matter to have a coelom?

From a developmental standpoint a coelom is a pretty sophisticated object. It's not just a fluid-filled cavity, in full form. It's also a system of muscles, and nerves to control them, that let it act as an internal skeleton. It's also a "skin" capable of absorbing and holding fluid pressure, and preventing unwanted leakage. If it comes in several connected parts, there have to be sphincters between the parts so fluid will only pass between when wanted. Without these, a coelom doesn't really do an animal much good. With them all, it's a pretty sophisticated pattern.

If the early bilaterians didn't have coela, what did they have?

My guess is that the earliest system used by animals was something that combined the characteristics of springy cartilage and simple muscle. These muscles weren't used all the time, but only for emergencies. Being thin, and lighter than the sort of heavy cartilage used by land animals, it was capable of diffusing both glucose and lactic acid enough to supply the needs of the cells that maintained the structure as well as the muscle cells. Note that this would have been extreme "white meat": they would depend almost entirely on anaerobic processes. Unlike oxygen, the relative concentrations of glucose and lactic acid could have been manipulated by cells outside this "myoskeleton", especially those on the surface, where they would have access to outside oxygen and could keep up the other side of the Cori cycle.

Most movement would have been achieved by cilia, as is the case for Ctenophores today. Ctenophores are generally considered the earliest-branching of the eumetazoans, and in this respect they may well be typical of the earliest. Although they have discreet muscles separate from the cartilage-like stiffening, this is likely a later development, although it probably took place prior to the branching.

The advantage of this system is that it could easily evolve from an even earlier one in which there was a simple static body stiffened by springy cartilage, and moved by cilia. Nerve cells would probably have begun as a system of controlling ciliar movement.


Ctenophores are generally biradial, which is a special form of radial symmetry with an index of two (D2 in the linked explanation: don't blame me it was the best I could find). In biradial symmetry, there are two symetrical reflection planes at right angles. In Ctenophores these planes are both parallel to the oral/aboral line, one passing through the tentacles and one passing through the body equidistant from them. The symmetry is not complete, since the anal pores appear to be asymmetrical in many species, however it is as good as the "bilateral" symmetry of humans, for instance, with our heart more on one side than the other (not to mention differences in the lungs, liver, etc.)

Modern ctenophores also have in imposed 8-fold symmetry on their cilia bands and the major portions of their gut.

The Cnidarians are generally known for their radial symmetry, however their larvae, called planulae, are also have biradial symmetry, as does the polyp form. Indeed, the larger-indexed radial symmetry of the medusa is also overlaid on a basic biradial pattern.

In a paper5 published a few years ago, it was demonstrated that the larvae of the sea anemone Nematostella vectensis actually had bilateral symmetry rather than biradial, at least in respect to the expression of certain very important genes (Hox and Dpp). Does this mean that the Cnidarians are actually bilaterians?

Symmetry and Control

As mentioned above, the "bilateral" symmetry of most bilaterians, including humans, is superficial. Our internal organs don't entirely reflect this symmetry, and neither do our preferences regarding which hand to use for what. Indeed, the development of language seems to have intensified the differences between the two halves of the brain, compared to our closest relatives.

To understand this, we need to consider the nervous system, and specifically its purpose. The sponges have no nerves, no muscles, and no symmetry. But with the advent of movement (excluding the placozoa, of which we know too little), we find symmetry. The ability to define the form of specific body parts is easily combined with the specification of more than one with the same form: why develop a separate plan for each member when one plan can be used for many? The same can be said of controlling these members: if your left tentacle is identical to your right, the same set of built-in patterns can be used with each. Thus, we find symmetry primarily in the outer forms of animals that use movement.

But that symmetry is superficial, and most bilaterians, such as mammals10 and everbody's favorite nematode Caenorhabditis elegans,11 have asymmetries that depend on developmental differences in gene expression.

Figure 2: crab with asymmetrical claws. (From Pre-Requisite Meta Principles in a Batesonian Epistemology

Indeed, this can be seen logically, since even if an animal is identical left-to-right down to the individual nerve cells, it can't do very well reacting to a threat on the right without knowing it's not on the left. Nerves have to cross the center-line to coordinate use of muscles (or even swimming cilia), and to do that they have to know which side they're on, and which way they're going.

The same is true for animals with radial symmetry. Even if they are perfectly symmetrical in form, their behavior depends on nerve cells whose axons knew which index of the symmetry they had to grow into, and brains or even distributed nerve nets that can distinguish the location of threats or prey and drive activity accordingly.

Thus, evidence of asymmetry in biradial animals such as cnidarians doesn't necessarily make them bilateral, any more than the crab above is no longer a bilaterian. We can take it for granted that, one way or another, any animal with nerves and muscles has some way for its cells to know which side of the body they're on.


One of the major features used to classify animals from early days has been the intestinal system. Cnidarians have a blind gut, unlike most bilaterians. Ctenophores technically have something called anal pores, however they are at the back of the gullet, not at the end of the stomach, and they appear not to be used for much (if any) excretion of undigested matter, which exits through the mouth. The Acoela also have a blind gut, strongly suggesting that this was the case for the ubilaterian. How much does this matter?

In fact, probably not much. In my opinion, the importance of a "pass-through" gut for early animals is much overrated. Ctenophores and cnidarians have no trouble moving digesting food around their blind guts, and the digestive process could even involve various stages of changing pH as is true for most animals with pass-through guts. Not only that, but the mutation that creates a new "hole" in an existing gut is probably a very small and common one for small, simple creatures.

Where the difference comes in is when the gut has to maintain a high pressure. We note the most cnidarians have a sphincter so they can use the pressure in their gut as a skeleton. But the bilaterians, when they've needed such skeletons, have almost always evolved coela, keeping the gut free for digestion. The need to contain pressure in the gut is almost certainly related to the use of enteric bacteria. The question is, when did this develop?

Cnidarians are all carnivores, and meat is much easier to digest than plant matter, especially without the help of bacteria. So are ctenophores. It seems likely that the ubilaterian also lacked intestinal flora, so it probably fed on protozoa or smaller animals.

The Lignin Revolution

When it comes to digesting plant matter, we have to consider lignin, "a complex chemical compound most commonly derived from wood, and an integral part of the secondary cell walls of plants and some algae." Continuing to quote Wiki, "[l]ignin is indigestible by animal enzymes, but some fungi and bacteria are able to secrete ligninases which can biodegrade the polymer. The details of the biodegradation are not well understood." Lignin used to be considered unique to green algae, from which land plants are descended, but have just this year been reported12 to be present in red algae as well. To quote from the discovering article "The finding of secondary walls and lignin in red algae raises many questions about the convergent or deeply conserved evolutionary history of these traits, given that red algae and vascular plants probably diverged more than 1 billion years ago."

The key here is that the need to use enteric bacteria to digest lignins put a need for high-pressure guts on any animal that ate them. One of the most important aspects of lignins is that they protect plants from ultraviolet radiation. This means they can float at the surface (and come out on land), without as much (if any) damage.

I'm proposing that at some point prior to the Cambrian there was a massive expansion of green algae (and perhaps red algae as well) with lignin-infused cellulose which could not be digested without the help of bacteria. This, in turn, induced a major requirement for "high-pressure guts" on many diverse animals. The bilaterians were already diverging, and several lineages already had "pass-through" guts, an innovation easy enough to get (if not all that valuable) prior to the need to contain high pressures. However, once many lineages had evolved high-pressure guts, it became much harder to evolve the "pass-through" guts since this would involve the need for another sphincter as well.

Of the various animals with blind guts that evolved sphincters, only the cnidarians, and perhaps the ancestors of Platyhelminthes, survived. Once developed and refined, the pass-through gut with bacterial help offered an "assembly line" approach to digestion that was generally better than anything that could be done with a blind gut.

Egger, B., Steinke, D., Tarui, H., De Mulder, K., Arendt, D., Borgonie, G., Funayama, N., Gschwentner, R., Hartenstein, V., Hobmayer, B., Hooge, M., Hrouda, M., Ishida, S., Kobayashi, C., Kuales, G., Nishimura, O., Pfister, D., Rieger, R., Salvenmoser, W., Smith, J., Technau, U., Tyler, S., Agata, K., Salzburger, W., & Ladurner, P. (2009). To Be or Not to Be a Flatworm: The Acoel Controversy PLoS ONE, 4 (5) DOI: 10.1371/journal.pone.0005502

MARTONE, P., ESTEVEZ, J., LU, F., RUEL, K., DENNY, M., SOMERVILLE, C., & RALPH, J. (2009). Discovery of Lignin in Seaweed Reveals Convergent Evolution of Cell-Wall Architecture Current Biology, 19 (2), 169-175 DOI: 10.1016/j.cub.2008.12.031

Links: (These aren't in any particular sequence, and not all are called out in the text, although I read all of them in preparing this post. Use the back key to return from where you came if you clicked on a footnote.)

1. To Be or Not to Be a Flatworm: The Acoel Controversy

2. The dawn of bilaterian animals: the case of acoelomorph flatworms

3. Hox and ParaHox genes in Nemertodermatida, a basal bilaterian clade

4. Improvement of molecular phylogenetic inference and the phylogeny of Bilateria

5. Origins of Bilateral Symmetry: Hox and Dpp Expression in a Sea Anemone (Requires free registration)

6. Back in time: a new systematic proposal for the Bilateria

7. Acoel development supports a simple planula-like urbilaterian

8. Acoel Flatworms Are Not Platyhelminthes: Evidence from Phylogenomics

9. Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum

10. The left-right axis in the mouse: from origin to morphology

11. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans

12. Discovery of Lignin in Seaweed Reveals Convergent Evolution of Cell-Wall Architecture


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