Xenoturbella and Xenacoelomorpha

Xenoturbella, Acoela, and Nemertodermatida are worm-like simple bilateral animals, which might give insights into the earliest steps in the evolution of Bilateria. Phylogenomic analyses (Philippe et al. 2011; Cannon et al. 2016) and some ultrastructural characters (Franzén & Afzelius 1987; Lundin 1998) group them into a monophyletic group, which has been named Xenacoelomorpha (Philippe et al. 2011; Tyler & Schilling 2011).

Xenoturbella has been kind of a puzzle for zoologists since it was described in 1949. First considered to be a primitive turbellarian flatworm, occasionally affiliated with Hemichordata, suggested to be a sister group to other bilaterians, for a moment mistaken for a mollusc, then suggested to be a deuterostome, then again together with Acoelomorpha (Acoela and Nemertodermatida) as a sister group to Bilateria, and then back to deuterostome affinity, as a sister group to Ambulacraria (Echinodermata and Hemichordata) (Telford 2008; Hejnol et al. 2009; Philippe et al. 2011). It is exciting that four new species of Xenoturbella have now been found in the Pacific ocean (Rouse et al. 2016). Before, only one small (up to 4 cm) species (X. bocki) was known from the west coast of Sweden (the second, X. westbladi, from the same place is probably the same species). Three of the new species are much bigger than X. bocki, some of them 20 cm or longer, but all are otherwise anatomically and in their habits (feeding on bivalves on the muddy ocean floor) quite similar to each other, which is also consistent with the genetic data. I heard about a new large Xenoturbella species found in the Pacific in 2010 while at EDIT taxonomy course in Kristineberg, Sweden. Sounded pretty unbelievable. I was hoping that this amazing new discovery will help to solve the phylogenetic position of Xenoturbella and Xenacoelomorpha more reliably, but it seems that the debate will continue for years to come.

Rouse et al. (2016) gathered also phylogenomic data for one of the new species and sequenced complete mitochondrial genomes of all the new species. Their phylogenetic analyses were incongruent to each other. Phylogenomic analyses based on nearly 1200 nuclear protein coding genes found Xenacoelomorpha (composed in this dataset of one Acoela and two Xenoturbella species) as sister group to other Bilateria (Nephrozoa) (using site homogeneous models) or as a sister group to Protostomia (using site heterogeneous CAT model). Analyses based on mitochondrial proteins grouped Xenacoelomorpha (4 acoels and 4 xenoturbellid species) with deuterostomes. In the same issue of Nature where Rouse et al's paper was published, Cannon et al. (2016) investigated the placement of Xenacoelomorpha more thoroughly, although using only one Xenoturbella species, but with many more Acoela species (7) and including Nemertodermatida (4 species). Cannon et al. (2016) added impressive amount of new transcriptome data (including for Xenoturbella), which enabled them to have pretty complete datasets for phylogenetic analyses (phylogenomic datasets tend to be gappy if not based on fully sequenced genomes). Cannon et al. (2016) results were much more consistent compared to Rouse et al. (2016), finding support only for sister-group relationship between Xenacoelomorpha and Nephrozoa (all other Bilateria, hypothetically having ancestrally nephridia in contrast to Xenacoelomorpha, which lack them). However, when fast-evolving acoelomorphs where excluded (retaining only clearly slower evolving Xenoturbella), statistical support for Nephrozoa and Deuterostomia decreased (from 99–100% to 81% in both cases). Unfortunately, Cannon et al. (2016) did not analyse this dataset with more complex CAT model and I suspect if they had, support for Nephrozoa and Deuterostomia would have disappeared entirely and Xenoturbella might have jumped next to Ambulacraria (as in Philippe et al. 2011). Cannon et al. (2016) did analyze their main dataset (which included Acoelomorpha) also with CAT model fully supporting Nephrozoa and Deuterostomia, but the internal branches leading to Nephrozoa and Deuterostomia of the resulting phylogenetic tree were clearly shorter (barely visible in the published figure) than in the analyses using simpler phylogenetic models. Simpler site homogeneous models underestimate the amount of sequence evolution compared to site heterogeneous models (like CAT) and can therefore produce artefactual groupings (grouping of fast-evolving, long-branch taxa with each other or with a distant out-group, regardless of their actual phylogenetic affinities). It could be that the fast-evolving Acoelomorpha (which is clearly evident in the long branches they display in phylogenetic analyses, the shortest ones perhaps still about twice as long as the Xenoturbella branch) caused the whole Xenacoelomorpha to shift artefactually at the base of Bilateria, away from more slowly evolving Deuterostomia and this way creating the Nephrozoa. CAT model was able to shorten the branches supporting monophyly of Nephrozoa and Deuterostomia, but not entirely to overcome possible non-phylogenetic signal present in the fast-evolving Acoelomorpha.

In conclusion, I think it is too early to exclude deuterostome affinity of Xenacoelomorpha. Curiously, while looking at the pictures of the new large species of Xenoturbella, I thought that they looked a bit like enteropneusts (Hemichordata). Could it be that the ring furrow of Xenoturbella, which divides the body into the head and tail region, is homologous to the collar (or to part of it) of Hemichordata (Deuterostomia: Ambulacraria)?

References

Cannon JT, Vellutini BC, Smith III J, Ronquist F, Jondelius U, Hejnol A (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530: 89–93. doi: 10.1038/nature16520

Franzen A, Afzelius BA (1987) The ciliated epidermis of Xenoturbella bocki (Platyhelminthes, Xenoturbellida) with some phylogenetic considerations. Zoologica Scripta 16: 9–17. doi: 10.1111/j.1463-6409.1987.tb00046.x

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. Proceedings. Biological sciences / The Royal Society 276: 4261–4270. doi: 10.1098/rspb.2009.0896

Lundin K (1998) The epidermal ciliary rootlets of Xenoturbella bocki (Xenoturbellida) revisited: new support for a possible kinship with the Acoelomorpha (Platyhelminthes). Zoologica Scripta 27: 263–270. doi: 10.1111/j.1463-6409.1998.tb00440.x

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. doi: 10.1038/nature09676

Rouse GW, Wilson NG, Carvajal JI, Vrijenhoek RC (2016) New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature 530: 94–97. doi: 10.1038/nature16545

Telford MJ (2008) Xenoturbellida: the fourth deuterostome phylum and the diet of worms. Genesis 46: 580–586. doi: 10.1002/dvg.20414

Tyler S, Schilling S (2011) Phylum Xenacoelomorpha Philippe, et al., 2011. In: Zhang, Z.-Q. (Ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148: 24–25.