Acoelomorpha: A Phylogenetic Headache

by Piter Kehoma Boll

Take a look at these guys:

Green worms Symsagittifera roscoffensis (Graff, 1891). Photograph by Vincent Maran. Extracted from doris.ffessm.fr

It’s a member of the group Acoelomorpha, animals which are still a puzzle in phylogeny. That means no one knows for sure where in the animals’ evolutionary tree they are exactly.

But first, let’s take a look at what makes an acoelomorph.

Those little guys are small worms, usually measuring less than 1 mm in length and living in marine or brackish waters or as symbionts. There are two groups of acoelomorphs: Acoela and Nemertodermatida. Acoels are the simplest ones; they have a mouth, but lack a gut, so that the food ingested goes directly to the internal tissues. In Nemertodermatida, there is a blind gut, i.e., with only one opening, like in the primitive cnidarians or in flatworms. In fact, they were initially classified as flatworms, but several features later challenged their position inside this phylum. The main differences are:

• Acoelomorphs have an epidermis (“skin”) with cilia whose roots are interconnected in a hexagonal pattern, while other flatworms have independent cilia.
• Acoelomorphs lack protonephridia (primitive kidney-like organs) and all other groups of animals have at least one of those or more complex organs with similar function.
• While flatworms and all other protostomes (arthropods, annelids, mollusks, nematodes…) have ventral nerve cords and deuterostomes (chordates, echinoderms…) have dorsal ones, in acoelomorphs there are several nerve cords distributed radially along the body length.

Distribution of nerve chords in Acoelomorpha, Protostomia and Deuterostomia. Picture by myself, Piter K. Boll.

Analyzing such features, it seems obvious that Acoelomorpha is a basal group of bilateral animals and may be the reminiscent of a primitive group of animals later almost completely extinct by their most complex descendants, the true protostomes and deuterostomes. The original radially-distributed nerve cords were simplified in dorsal or ventral ones in higher groups but remained radial in Acoelomorpha.

Several phylogenetic studies indicate that Acoelomorpha is indeed a basal group of bilateral animals. They also lack several important Hox genes (responsible for determining body plan and organs’ distribution in animals) and it is quite unlikely that they would have lost most of them by secondary simplification.

Another group of simple animals, the Xenoturubellida, was sometimes proposed as a sister group for Acoelomorpha. Their proximity would be explained by several shared features, mainly the simple nervous system, the lack of a stomatogastric (mouth-gut) system, the structure of the epidermal cilia and the unusual fact that, in both groups, epidermal degenerated cells as resorbed in the gastrodermis.

A Xenoturbella worm. Photograph extracted from bioenv.gu.se/english/staff/ Hiroaki_Nakano_eng/

The group Xenoturbellida, however, has been placed in Deuterostomia in some molecular studies and recently Philippe et al. 2011 proposed that Acoelomorpha would also belong to the Deuterostomia! But how could such a thing be possible when they obviously have primitive and unique features, like the radially placed nerve cords? The group’s explanation is that Acoelomorpha, as well as Xenoturbellida, have a sequence of microRNA (miR-103/107/2013) which is exclusive to Deuterostomia, so they would also be deuterostomes.

But wait a minute! What do they mean by “exclusive to Deuterostomia”? It means that that microRNA sequence is found in deuterostomes, but not in protostomes. Now think with me. We have 4 bilateral groups here: Acoelomorpha, Xenoturbellida, Deuterostomiaa and Protostomia. If you look at them this way, we can see that the statement “miR-103/107/2013 is exclusive to Deuterostomia” is false. The truth is that this sequence is absent in Protostomia but present in all other groups. Wouldn’t it be more logical to think that, instead of deuterostomes acquiring this sequence, what really happened is that it was a primitive microRNA and protostomes have lost it?

If you consider Xenoturbellida and Acoelomorpha inside Deuterostomia, you have to assume that they passed through a huge simplification, and you maintain the radial nerve cords unexplained. Now if you think of them as primitive groups, the only thing necessary is to analyze protostomes as having lost a microRNA sequence. Quite a simpler explanation which doesn’t let open gaps.

Phylogenetic position of Acoelomorpha and Xenoturbellida according to Philippe et al. 2011. It means that (1) the bilaterians’ ancestor had a complex set of Hox genes, being a complex animal; (2) miR-103/107/2013 appeared in an ancestor of true Deuterostomes+Xenacoelomorpha (Xenoturbellida + Acoelomorpha); (3) Xenacoelomorpha passed through a huge loss of Hox genes, loss of most internal organs and a mysterious set of radial nerve cords appear. Very complicated.

Phylogenetic position of Acoelomorpha and Xenoturbellida according to Boll et al. 2013 (that’s me!) based on a review of previous studies, as a basal group. It means that (1) the bilaterian’s ancestor was a simple animal, with a simple set of Hox genes, having miR-103/107/2013 and radial nerve cords; (2) the set of Hox genes became more complex and the nerve cords where simplified to either dorsal or ventral; (3) miR-103/107/2013 is lost in Protostomia. Way simpler.

You can read more in the references listed below.

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References:

Boll, P., Rossi, I., Amaral, S., Oliveira, S., Müller, E., Lemos, V., & Leal-Zanchet, A. (2013). Platyhelminthes ou apenas semelhantes a Platyhelminthes? Relações filogenéticas dos principais grupos de turbelários. Neotropical Biology and Conservation, 8 (1), 41-52 DOI: 10.4013/nbc.2013.81.06

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

Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G., Edgecombe, G., Martinez, P., Baguna, J., Bailly, X., Jondelius, U., Wiens, M., Muller, W., Seaver, E., Wheeler, W., Martindale, M., Giribet, G., & Dunn, C. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society B: Biological Sciences, 276 (1677), 4261-4270 DOI: 10.1098/rspb.2009.0896

Moreno, E., Nadal, M., Baguñà, J., & Martínez, P. (2009). Tracking the origins of the bilaterian patterning system: insights from the acoel flatworm. Evolution & Development, 11 (5), 574-581 DOI: 10.1111/j.1525-142X.2009.00363.x

Mwinyi, A., Bailly, X., Bourlat, S., Jondelius, U., Littlewood, D., & Podsiadlowski, L. (2010). The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis. BMC Evolutionary Biology, 10 (1) DOI: 10.1186/1471-2148-10-309

Philippe, H., Brinkmann, H., Copley, R., Moroz, L., Nakano, H., Poustka, A., Wallberg, A., Peterson, K., & Telford, M. (2011). Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature, 470 (7333), 255-258 DOI: 10.1038/nature09676