Xenoturbellida

Xenoturbellida is the name of a monogeneric phylum erected to accommodate Xenoturbella bocki and X. westbladi; pictured above is X. bocki (Telford, 2008). It’s of special interest for animal phylogeny because of its uncertain position among the basal bilaterians, if not within the deuterostomes. This post is an introduction to the organism and its phylogenetic placement.

First off, it’s necessary to establish that Xenoturbella is indeed a unique animal deserving of its own phylum. Ax (1995) lists four autapomorphies:

  • Epidermal cillia with two parallel roots.
  • Cilliated epidermal cells with support fibril made from bundles of filaments.
  • Subepidermal membrane complex comprising an outer and inner basal lamina and striped filaments in the center.
  • Intraepidermal statocyst with freely-moveable monocilliary cells floating inside it.

Xenoturbella is a wormy marine animal, inhabiting soft substrates up to 100 m deep. It’s white, up to 3 cm long, with conical extremities and a slightly-flattened body covered in cillia (except for an area in the middle of the body). Its epidermis is unusually thick, hence the need for the support fibrils.

The figures above show the anatomy of Xenoturbella, from Telford (2008). The abbreviations below refer to them.

A mouth (m) is found near the middle of the animal, leading directly into the stomach (gc). There is no pharynx and no anus.

Its nervous system is a simple basiepithelial nerve net (np), with no sign of a brain or any true nerve cords. The statocyst (st) at the anterior end of the animal has a nervous plexus associated with it, but that is the only form of nervous system centralisation found. The statocyst itself is enclosed in a capsule, the interior of which contains many monocilliary cells floating around.

Two muscular system are found. The main one is formed by the autapomorphic subepidermal membrane complex running across the entire body (musc), where the filaments are differentiated into longitudinal and circular muscles (lm, cm), allowing peristaltic movement. A second system is found around the stomach (rm).

Their reproduction is very simple. They’re hermaphrodites with no gonads, genital openings or copulation rituals. Eggs and sperm originate in the parenchyma surrounding the intestine (int). Eggs break into the stomach and are transferred to the mouth and released (Beklemishev, 1969); the same is presumed to happen to sperm, although this hasn’t been observed.

When Xenoturbella bocki was first described by Westblad (1949), he placed it as a turbellarian platyhelminth, a hypothesis that has fallen out of favour. Support can be found for them being related to acoelomorphs (Telford, 2008). Shared characters that are potentially apomorphic for such a clade include a ventral mouth, hermaphroditism (plesiomorphic), lack of coeloms, and the arrangement of the nervous system (see Westblad, 1949). The problem is that all of these can easily evolve convergently; more detailed characters involving the structure of the cillia don’t stand up to scrutiny. This relationship, if true, would be very important, since acoels are purported to be pretty basal in bilaterian phylogeny (Ruiz-Trillo et al., 1999) and thus critical to understanding the evolution of animals.

However, what phylogenomics shows us nowadays is that the Acoelomorpha and Xenoturbellida are sisters in the deuterostomes (Philippe et al., 2011), echoing earlier results based on ESTs from the same group of (excellent) researchers (Philippe et al., 2007). The clade is referred to as the Xenacoelomorpha. This is significantly different from having them at the base of the Bilateria, with the main implication being that the evolution of the deuterostomes is one that involves plenty of character losses causing extreme morphological disparity – think of how profoundly different echinoderms, hemichordates, chordates, tunicates, acoels and Xenoturbella are.

The current consensus view, based mostly on nuclear genes, is that Xenoturbella belongs somewhere in the Deuterostomia (Bourlat et al., 2003), most probably as the sister group to the Ambulacraria (as seen in the diagram above, from Telford & Littlewood (2009); see Bourlat et al. (2006)). Mitochondrial genes support them as basal deuterostomes (Perseke et al., 2007). Whether the acoels end up joining them there is still up for more analysis and debate, but given how impressive modern phylogenomic results have been, I personally support it.

An interesting alternative, again from phylogenomics, is that Xenoturbella is itself an acoelomorph (Hejnol et al., 2009). In that study, the Acoelomorpha were recovered as basal bilaterians.

So, to summarise the views for the position of xenoturbellids proposed so far:

  1. Turbellarian flatworms, based on morphology, by Westblad (1949). Disregarded hypothesis.
  2. Sister to Acoelomorpha near the base of the Bilateria, based on molecular evidence.
  3. In the Acoelomorpha near the base of the Bilateria, based on phylogenomics, Hejnol et al. (2009).
  4. Basal Deuterostomia, based on mitochondrial data, Perseke et al. (2007).
  5. Sister to the Ambulacraria (Hemichordata + Echinodermata), based on molecular data, Bourlat et al. (2006).
  6. Clading with the Acoelomorpha as sister to the Ambulacraria, based on phylogenomics, Philippe et al. (2011).

To me, this entire debate revolves around methodology. Simple sequence data, mitochondrial or nuclear, don’t support a close relationship with acoels; phylogenomics does (either as a sister group or as a parent taxon). The way to resolve such a conflict isn’t by simply running more analyses with more taxa or sequences, but to try and understand why this discrepancy exists. For example, we know that molecular evolution rates in acoels and xenoturbellids are rather wonky. How does this affect the analysis? Are there any biases in molecular evolution in the relevant clades (any codon positions or amino acid more prone to change)? These are the questions that have to be asked before wasting more computing power. Once we have the answers, we can build better tools to incorporate the knowledge. Of course, this work is already happening, this isn’t an original thought.

References:

Ax P. 1995. Das System der Metazoa I.

Beklemishev WN. 1969. Principles of Comparative Anatomy of Invertebrates: Organology.

Bourlat SJ, Nielsen C, Lockyer AE, Littlewood DTJ & Telford MJ. 2003. Xenoturbella is a deuterostome that eats molluscs. Nature 424, 925-928.

Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thomdyke M, Nakano H, Kohn AB, Heyland A, Moroz LL, Copley RR & Telford MJ. 2006. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444, 85-88.

Giribet G, Dunn CW, Edgecombe GD & Rouse GW. 2007. A modern look at the Animal Tree of Life. Zootaxa 1668, 61-79.

Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Müller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G & Dunn CW. 2009. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. B 276, 4261-4270.

Perseke M, Hankeln T, Weich B, Fritzsch G, Stadler PF, Israelsson O, Bernhard D & Schlegel M. 2007. The mitochondrial DNA of Xenoturbella bocki: genomic architecture and phylogenetic analysis. Theory in Bioscience 126, 35-42.

Philippe H, Brinkmann H, Martínez P, Riutort M & Baguñà J. 2007. Acoel flatworms are not Platyhelminthes: evidence from phylogenomics. PLoS ONE 2, e717.

Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ & Telford MJ. 2011. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470, 255-258.

Telford M. 2008. Xenoturbellida: the fourth deuterostome phylum and the diet of worms. Genesis 46, 580-586.

Rohde K, Watson N & Cannon LRG. 1988. Ultrastructure of epidermal cilia of Pseudactinoposthia sp. (Platyhelminthes, Acoela); implications for the phylogenetic status of the Xenoturbellida and Acoelomorpha. Journal of Submicroscopic Cytology 20, 759-767.

Ruiz-Trillo I, Riutort M, Littlewood DT, Herniou EA & Baguna J. 1999. Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science 283, 1919-1923.

Telford MJ & Littlewood DTJ. 2009. Animal Evolution: Genomes, Fossils, and Trees.

Westblad E. 1949. Xenoturbella bocki n. g. n. sp., a peculiar, primitive Turbellarian type. Arkiv for Zoologi 1, 11-29.

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