Acoela

Convolutriloba retrogemma, copyright AquariaNR.

Belongs within: Xenacoelomorpha.
Contains: Actinoposthiidae, Convolutidae.

Our faceless cousins?
Published 13 August 2007
Acoel anatomy, from Answers.com.


A paper has appeared in PLoS One by Philippe et al. on the phylogenetic position of Acoela in the animal evolutionary tree (freely available at the link). Acoela are a smallish group (only a few hundred described species) of marine “worms”, superficially similar to flatworms (Platyhelminthes) in appearance. They lack a proper gut—the mouth in the diagram above opens into a pharynx leading to a shapeless mass of digestive cells, where individual cells take up food particles and digest them via phagocytosis. In the past they were included in Platyhelminthes, and still appear as such in textbooks (which are always out of date), the entire complex being regarded as the basalmost of all bilaterian phyla. However, though Acoela resemble flatworms in features such as absence of a coelom or through-gut (the features previously regarded as primitive for bilaterians), recent molecular investigations have positioned them well away from the Platyhelminthes. Meanwhile, the Platyhelminthes cluster within the Protostomia, implying that their supposed primitive features instead represent derivations from more complex organisms. I am not aware of any attempts so far to explain exactly why and how Platyhelminthes came to dispense seemingly integral features like an anus, but they seem to have done exactly that.

The Acoela are a different story, though. Molecular analyses have placed Acoela at the very base of the bilaterian tree, below the divergence of deuterostomes and protostomes. With this topography, the primitive features of Acoela might indeed be primitive, making this a potentially significant taxon in understanding how the triploblastic Bilateria arose from their diploblastic, radial ancestors (probably similar to modern Cnidaria). Another small marine worm group*, the Nemertodermatida, shares a number of features with Acoela and the two are usually united as Acoelomorpha. However, the monophyly of Acoelomorpha is not certain (Ruiz-Trillo et al. 2002), and could do with further investigation. The paper I’m dealing with today only deals directly with Acoela.

*If you’re wondering if “small marine worm group” means “small group of marine worms” or “group of small marine worms”, both are equally applicable.

Planula, from Fiorenza Accordi.

The supposed position of Acoelomorpha as basalmost bilaterians is particularly interesting because Acoelomorpha are not unlike in appearance to a cnidarian planula larva (example shown above). As such, they give credence to the idea that Bilateria may have originated from the development of sexual maturity in a planuloid larva (Baguñà & Riutort 2004b) [As an aside, the Wikipedia page for “planula” previously stated that planulae are incapable of feeding—this only appears to be true for Medusozoa, as Anthozoa have feeding planulae.]

Enter Philippe et al., who used a positively huge molecular data set derived from 68 protein-coding genes to test the position of Acoela, using the exemplar Convoluta pulchra. Because Acoela show a rapid evolutionary speed, making long-branch attraction potentially a significant problem, Philippe et al. used an analytical model that is supposedly more resistant to long-branch attraction. Their final tree agreed with previous studies that Acoela were not related to Platyhelminthes, but disagreed about their position outside the deuterostome + protostome clade. Instead, Convoluta appeared as the sister group to Deuterostomia, a previously unsuspected position.

Under an alternative model, Convoluta appeared in its more traditional position with Platyhelminthes, but this is almost certainly due to long-branch attraction. Platyhelminthes had the longest branches in the analysis (other than Convoluta itself), and their removal caused Convoluta to madly leap away and latch itself onto the chordate Oikopleura, possessor of the next-longest branch. Also, Philippe et al. were able to identify the presence in Convoluta of the gene for guanidinoacetate N-methyltransferase. This gene is found in all animals other than protostomes, but has been lost in the latter. Strangely enough, when the analysis was run without including non-bilaterians, Convoluta became the sister in Deuterostomia of the worm-like Xenoturbella, which is the sister of the Ambulacraria (hemichordates and echinoderms). Xenoturbella resembles Acoela in lacking a through-gut and in the ultrastructure of the epidermal ciliary rootlets, so this is not outside the bounds of possibility.

Nevertheless, I remain somewhat skeptical of the overall result. Bootstrap support for the result was low (only 34%), but a position for Convoluta outside the deuterostome + protostome clade (Eubilateria) got even less support (only 7%). In fact, bootstrap support was pretty low overall within the Deuterostomia (in contrast, Protostomia [including Chaetognatha as basalmost branch] had a bootstrap result of 99%). I feel compelled to chant the usual mantra of all studies—”we need more data!” (though the authors of a study that did, after all, compare 11,959 positions might reply with “for the love of…how much bloody data do you want?”). One particular comment in the paper got my attention:

In more conceptual terms, the position of acoels out of the Platyhelminthes should warn us against the naive view that considers some features as ‘lost’, ‘absent’, or ‘reduced’ in clades (e.g. acoels) than might never have had them in the first place.

However, if Acoela are indeed related to Deuterostomia, then I would feel that they are almost certainly secondarily reduced. It is much easier to regard characters shared between eubilaterians, such as fully formed brain ganglia and the through-gut (Baguñà & Riutort 2004b), as lost in Acoelomorpha rather than gained independently in deuterostomes and protostomes (or even protostomes, chordates and ambulacrarians, if Acoelomorpha are together with Xenoturbella [which also lost these features] the sister to Ambulacraria).

I was going to mention Hox genes here too. Baguñà & Riutort (2004b) had a nice tree to support the basal position of acoelomorphs that showed Acoelomorpha with only one central Hox gene and one posterior Hox gene, while the basal number for Eubilateria was four central and at least two posterior Hox genes. However, I then noticed that the author list for the current paper included the same two authors, Baguñà and Riutort. Now, the ideal rule in science is to “believe the data, not the reporter”, but I couldn’t help wondering if they now knew something that I didn’t (quite possible, after all). A quick search doesn’t reveal much change for Acoela—Nemertodermatida do have two central Hox genes, but as the second cannot be readily attached to any of the missing eubilaterian genes, it may represent an independent duplication (Jiménez-Guri et al. 2006). However, an apparently not-yet-published study available online by Fritzsch et al. found that Xenoturbella also had only two central Hox genes (though sequence analysis of said genes united them with other deuterostomes rather than acoelomorphs). As a result, if acoelomorphs are closer to deuterostomes than protostomes, I feel that the position in the restricted analysis as sister to Xenoturbella seems more likely than the position as sister to all Deuterostomia in the total analysis. At least that only requires one loss of the characters mentioned.

Gutless wonders
Published 8 March 2011
Congregation of Symsagittifera roscoffensis, photographed by Patrick Le Mao.

The Acoela are a distinct assemblage of marine worms ranging in size from the microscopic to a little over a centimetre in length. The name ‘Acoela’ means ‘without a cavity’, and refers to the lack of a proper gut in these animals. Instead, the mouth (which is situated on the underside of the animal) leads to a central vacuole surrounded by a syncytium (a multinucleate mass that is not divided into individual cells) that takes in nutritive particles by phagocytosis (engulfment by membrane folding, like how an Amoeba feeds). In many of the larger acoels, feeding is supplemented (or even largely superseded) by the presence of endosymbiotic algae that provide nutrients for their host worm (it is the algae that give the worms in the photo above their bright green colour). One particular family of acoels, the Solenofilomorphidae, live in anoxic sulfide sands, an environment that until the late 1960s was thought inimicable to animal life.

The panther worm Hofstenia miamia, photographed by Andreas Wallberg.

Acoels have received most attention in recent years due to debate about their relationships to other animals. Long included among the Platyhelminthes (flatworms), recent studies have indicated that acoels are not close relatives of that group (which is now placed as a derived lineage of Lophotrochozoa). It is generally accepted that acoels are most closely related to a similar group of marine worms called Nemertodermatida, and a few recent studies have also connected them with another marine worm Xenoturbella (Philippe et al. 2011). All three groups lack a through-gut, and a relationship between them seems credible. As regards the connection between this total group and other animals, there are three main options currently on the table: (1) Acoels and their relatives are the sister group (or, in some studies, successive sister groups) to all other bilaterians. This is perhaps the most popular position, and suggests that the simple morphology of acoels relative to other animals may be comparable to the ancestral morphology for bilaterians as a whole. (2) Some recent studies (e.g. Philippe et al. 2011) have recovered an alternative position for acoels within the deuterostomes, as sister to echinoderms + hemichordates. If so, the simple morphology of acoels would probably be derived from more complex ancestors. (3) Finally, there are still some studies (e.g. Dunn et al. 2008) whose results place acoels together with the Platyhelminthes among the Lophotrochozoa (generally as the sister to other Platyhelminthes). However, most current researchers seem to regard such results as due to long-branch attraction between the two groups.

Specimens of an unidentified species of acoel on coral, photographed by Teresa Zubi.

Within the Acoela themselves, recent studies have supported the association of larger species as a clade nested among the smaller species (Hooge & Tyler 2006). Many characters used in earlier classifications of the group, such as the presence of a pharynx or endosymbionts or the placement and numbers of genitalia*, have not always related well to recent molecular phylogenies, but other features such as the arrangement of muscles in the body wall have. One particularly notable feature has been the arrangement of microtubules in the spermatozoa, with successive reductions in the number of central microtubules (from the ancestral 9 + 2 arrangement, to 9 + 1, to 9 + 0) correlating strongly with molecular data (Hooge & Tyler 2006).

*I believe I’ve noted it before, but for all that organisms such as microscopic worms are usually regarded as morphologically ‘simple’ and ‘conservative’, you don’t find much variation among more ‘complex’ animals like mammals in the number of penises they have.

Systematics of Acoela
Acoela
|--ParatomellidaeBR04
| |--HesioliciumH01
| `--ParatomellaH01
| |--P. rubraMV04
| `--P. unichaeta Dörjes 1966H01
`--EuacoelaBR04
| i. s.: ActinoposthiidaeBR04
| AntigonaridaeBR04
| AntroposthidaeBR04
| ConvolutidaeBR04
| HallangidaeBR04
| HaploposthiidaeBR04
| |--Haploposthia vandula Hooge & Tyler 2001H01
| |--Parahaploposthia velvetum Hooge & Tyler 2001H01
| `--Haplogonaria Dörjes 1968H03
| |--H. arenaria (Ax 1959)H03
| |--H. pellita (Marcus 1951)H03
| |--H. stradbrokensis Hooge 2003H03
| |--H. syltensisK92
| `--H. viridisK92
| MyostomellidaeBR04
| NadinidaeBR04
| OtocelididaeBR04
| |--Notocelis gullmarensis (Westblad 1946)H01
| |--Philocelis brueggemanni Hooge & Tyler 2001H01
| |--Stomatricha Hooge 2003H03
| | `--*S. hochbergi Hooge 2003H03
| `--OtocelisH03
| |--O. luteolaH03
| `--O. sandara Hooge & Tyler 2001H01
| ProporusH01 [ProporidaeBR04]
| |--P. bermudensis Hooge & Tyler 2001H01
| `--P. lonchitus Dörjes 1971H01
| SolenofilomorphidaeBR04
| |--Solenofilomorpha funilisH96
| `--MyopeaH01
| TaurididaeBR04
|--DiopisthoporusCV16 [DiopisthoporidaeH01]
| |--D. gymnopharyngeusCV16
| `--D. longitubusCV16
`--+--HofsteniaCV16 [HofsteniidaeH01]
| `--H. miamiaCV16
`--+--Isodiametra [Isodiametridae]CV16
| `--I. pulchraCV16
`--+--MecynostomidaeH01
| |--Paedomecynostomum bruneum Dörjes 1968H01
| |--Mecynostomum filiferumA66
| |--EumecynostomumCV16
| | |--E. asterium Hooge & Tyler 2001H01
| | `--E. macrobursaliumCV16
| `--PseudmecynostomumH01
| |--P. folium Hooge & Tyler 2001H01
| `--P. phocum Hooge & Tyler 2001H01
`--+--Childia Graff 1910CV16, H01 [Childiidae]
| |--C. groenlandica (Levinsen 1879)H01
| `--C. submaculatumCV16
`--+--AnaperusH01 [AnaperidaeBR04]
| |--A. gardineri Graff 1911H01
| `--A. tvaerminnensisH01
`--SagittiferidaeH01
|--Antrosagittifera corallina Hooge & Tyler 2001H01
`--ConvolutrilobaCV16
|--C. hastifera Winsor 1990H03
|--C. longifissura Bartolomaeus & Balzer 1997H01
|--C. macropygaCV16
`--C. retrogemma Hendelberg & Åkesson 1988H03

Acoela incertae sedis:
Childianea coomerensis Faubel & Cameron 2001H03
Heterochaerus australis Haswell 1905H03
Waminoa litus Winsor 1990H03
Philachoerus johanniK92
Symsagittifera roscoffensisDH08
Daku Hooge 2003 [Dakuidae]H03
`--*D. woorimensis Hooge 2003H03
Polycanthus Hooge 2003 [Polycanthiidae]H03
`--*P. torosus Hooge 2003H03
Anapterus tvaerminnensisH96
Endocincta punctataH96

*Type species of generic name indicated

References

[BR04] Baguñà, J., & M. Riutorta. 2004. Molecular phylogeny of the Platyhelminthes. Canadian Journal of Zoology 82: 168–193.

Baguñà, J., & M. Riutort. 2004b. The dawn of bilaterian animals: the case of acoelomorph flatworms. BioEssays 26 (10): 1046–1057.

[CV16] Cannon, J. T., B. C. Vellutini, J. Smith, III, F. Ronquist, U. Jondelius & A. Hejnol. 2016. Xenacoelomorpha is the sister group to Nephrozoa. Nature 530: 89–93.

[DH08] Dunn, C. W., A. Hejnol, D. Q. Matus, K. Pang, W. E. Browne, S. A. Smith, E. Seaver, G. W. Rouse, M. Obst, G. D. Edgecombe, M. V. Sørensen, S. H. D. Haddock, A. Schmidt-Rhaesa, A. Okusu, R. M. Kristensen, W. C. Wheeler, M. Q. Martindale & G. Giribet. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745–749.

[H96] Haszprunar, G. 1996. The Mollusca: coelomate turbellarians or mesenchymate annelids? In: Taylor, J. D. (ed.) Origin and Evolutionary Radiation of the Mollusca pp. 1–28. Oxford University Press: Oxford.

[H01] Hooge, M. D. 2001. Evolution of body-wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). Journal of Morphology 249: 171–194.

[H03] Hooge, M. D. 2003. Two new families, three new genera, and four new species of acoel flatworms (Acoela, Platyhelminthes) from Queensland, Australia. Cahiers de Biologie Marine 44: 275–298.

Hooge, M. D., & S. Tyler. 2006. Concordance of molecular and morphological data: the example of the Acoela. Integrative and Comparative Biology 46 (2): 118–124.

Jiménez-Guri, E., J. Paps, J. García-Fernàndez & E. Saló. 2006. Hox and ParaHox genes in Nemertodermatida, a basal bilaterian clade. International Journal of Developmental Biology 50: 675–679.

[K92] Kozloff, E. N. 1992. The genera of the phylum Orthonectida. Cahiers de Biologie Marine 33: 377–406.

[MV04] Manylov, O. G., N. S. Vladychenskaya, I. A. Milyutina, O. S. Kedrova, N. P. Korokhov, G. A. Dvoryanchikov, V. V. Aleshin & N. B. Petrov. 2004. Analysis of 18S rRNA gene sequences suggests significant molecular differences between Macrodasyida and Chaetonotida (Gastrotricha). Molecular Phylogenetics and Evolution 30: 850–854.

Philippe, H., H. Brinkmann, P. Martinez, M. Riutort & J. Baguñà. 2007. Acoel flatworms are not Platyhelminthes: evidence from phylogenomics. PLoS ONE 2(8): e717. doi:10.1371/journal.pone.0000717

Philippe, H., H. Brinkmann, R. R. Copley, L. L. Moroz, H. Nakano, A. J. Poustka, A. Wallberg, K. J. Peterson & M. J. Telford. 2011. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470: 255–258.

Ruiz-Trillo, I., J. Paps, M. Loukota, C. Ribera, U. Jondelius, J. Baguñà & M. Riutort. 2002. A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians. Proceedings of the National Academy of Sciences of the USA 99 (17): 11246–11251.

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