Acoel Flatworms: Earliest Extant Bilaterian Metazoans, Not Members of Platyhelminthes

Ruiz‐Trillo, Iñaki; Riutort, Marta; Littlewood, D. Timothy J.; Herniou, Elisabeth A.; Baguñà, Jaume

doi:10.1126/science.283.5409.1919

Cited by 413 publications

(314 citation statements)

References 33 publications

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“…Our main aims were to test again the position of the 'acoelomorph' flatworms as early branching bilaterians (Ruiz-Trillo et al 1999 and to single out early branching phyla at the base of the three superphyla. Finally, and based on the growing consensus of cnidarians as true bilaterians Martindale 2005), a new systematic proposal for the Bilateria is suggested.…”

Section: Molecular Phylogeny Of the Bilateria: New Datamentioning

confidence: 99%

Back in time: a new systematic proposal for the Bilateria

Baguñà

Martinez

Paps

et al. 2008

Phil. Trans. R. Soc. B

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Conventional wisdom suggests that bilateral organisms arose from ancestors that were radially, rather than bilaterally, symmetrical and, therefore, had a single body axis and no mesoderm. The two main hypotheses on how this transformation took place consider either a simple organism akin to the planula larva of extant cnidarians or the acoel Platyhelminthes (planuloid-acoeloid theory), or a rather complex organism bearing several or most features of advanced coelomate bilaterians (archicoelomate theory). We report phylogenetic analyses of bilaterian metazoans using quantitative (ribosomal, nuclear and expressed sequence tag sequences) and qualitative (HOX cluster genes and microRNA sets) markers. The phylogenetic trees obtained corroborate the position of acoel and nemertodermatid flatworms as the earliest branching extant members of the Bilateria. Moreover, some acoelomate and pseudocoelomate clades appear as early branching lophotrochozoans and deuterostomes. These results strengthen the view that stem bilaterians were small, acoelomate/pseudocoelomate, benthic organisms derived from planuloid-like organisms. Because morphological and recent gene expression data suggest that cnidarians are actually bilateral, the origin of the last common bilaterian ancestor has to be put back in time earlier than the cnidarian-bilaterian split in the form of a planuloid animal. A new systematic scheme for the Bilateria that includes the Cnidaria is suggested and its main implications discussed.

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Section: Molecular Phylogeny Of the Bilateria: New Datamentioning

confidence: 99%

Back in time: a new systematic proposal for the Bilateria

Baguñà

Martinez

Paps

et al. 2008

Phil. Trans. R. Soc. B

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“…This is therefore one of the most important remaining problems in animal phylogenetics. Acoela has been recovered as the sister group to all other bilaterian animals in direct sequencing analyses, though their placement with respect to Nemertodermatida has been inconsistent (Ruiz-Trillo et al 1999Jondelius et al 2002;Wallberg et al 2007;Paps et al 2009). The position of acoels has not been resolved satisfactorily in previous EST-based analyses (Philippe et al 2007;Dunn et al 2008;Egger et al 2009).…”

Section: Introduction (A) Scalability In Phylogenomic Analysesmentioning

confidence: 99%

Assessing the root of bilaterian animals with scalable phylogenomic methods

et al. 2009

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A clear picture of animal relationships is a prerequisite to understand how the morphological and ecological diversity of animals evolved over time. Among others, the placement of the acoelomorph flatworms, Acoela and Nemertodermatida, has fundamental implications for the origin and evolution of various animal organ systems. Their position, however, has been inconsistent in phylogenetic studies using one or several genes. Furthermore, Acoela has been among the least stable taxa in recent animal phylogenomic analyses, which simultaneously examine many genes from many species, while Nemertodermatida has not been sampled in any phylogenomic study. New sequence data are presented here from organisms targeted for their instability or lack of representation in prior analyses, and are analysed in combination with other publicly available data. We also designed new automated explicit methods for identifying and selecting common genes across different species, and developed highly optimized supercomputing tools to reconstruct relationships from gene sequences. The results of the work corroborate several recently established findings about animal relationships and provide new support for the placement of other groups. These new data and methods strongly uphold previous suggestions that Acoelomorpha is sister clade to all other bilaterian animals, find diminishing evidence for the placement of the enigmatic Xenoturbella within Deuterostomia, and place Cycliophora with Entoprocta and Ectoprocta. The work highlights the implications that these arrangements have for metazoan evolution and permits a clearer picture of ancestral morphologies and life histories in the deep past.

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“…The acoel sequences appear with extremely long branches in the phylogenomics trees. In this regard, it is worth pointing that the branch on the acoel P. rubra in both our 18S rRNA and 13-gene animal phylogeny (Paps et al 2009b;Ruiz-Trillo et al 1999) appeared shorter than other animal clades. The lack of P. rubra in phylogenomic analyses conducted thus far is discouraging and we believe efforts to obtain additional molecular data from P. rubra, or other acoel taxa with slower evolutionary rates, should be encouraged.…”

Section: Perspectivesmentioning

confidence: 60%

“…The finding of acoels with slower rates of nucleotide substitution apparently settled the debate by overcoming the persistent LBA problem (Ruiz-Trillo et al 1999). In a taxon-rich analysis, we screened up to 18 different acoel taxa and removed those with faster evolutionary rates.…”

mentioning

confidence: 99%

“…In a taxon-rich analysis, we screened up to 18 different acoel taxa and removed those with faster evolutionary rates. When only the sequence of an acoel with similar evolutionary rates than the rest of animals (Paratomella rubra) was used, acoels appeared consistently and with strong nodal support as the sister group to the other Bilateria (Ruiz-Trillo et al 1999), far from the Platyhelminthes, which branched within Lophotrochozoa. Thus, a new evolutionary scenario emerged: acoels were situated as sister group to the rest of Bilateria, and Platyhelminthes as members of the Lophotrochozoa assemblage (Fig.…”

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confidence: 99%

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Acoelomorpha: earliest branching bilaterians or deuterostomes?

Ruiz‐Trillo

Paps

2015

Org Divers Evol

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The Acoelomorpha is an animal group comprised by nearly 400 species of misleadingly inconspicuous flatworms. Despite this, acoelomorphs have been at the centre of a heated debate about the origin of bilaterian animals for 150 years. The animal tree of life has undergone major changes during the last decades, thanks largely to the advent of molecular data together with the development of more rigorous phylogenetic methods. There is now a relatively robust backbone of the animal tree of life. However, some crucial nodes remain contentious, especially the node defining the root of Bilateria. Some studies situate Acoelomorpha (and Xenoturbellida) as the sister group of all other bilaterians, while other analyses group them within the deuterostomes which instead suggests that the last common bilaterian ancestor directly gave rise to deuterostomes and protostomes. The resolution of this node will have a profound impact on our understanding of animal/bilaterian evolution. In particular, if acoelomorphs are the sister group to Bilateria, it will point to a simple nature for the first bilaterian. Alternatively, if acoelomorphs are deuterostomes, this will imply that they are the result of secondary simplification. Here, we review the state of this question and provide potential ways to solve this longstanding issue. Specifically, we argue for the benefits of (1) obtaining additional genomic data from acoelomorphs, in particular from taxa with slower evolutionary rates; (2) the development of new tools to analyse the data; and (3) the use of metagenomics or metatranscriptomics data. We believe the combination of these three approaches will provide a definitive answer as to the position of the acoelomorphs in the animal tree of life.

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Acoel Flatworms: Earliest Extant Bilaterian Metazoans, Not Members of Platyhelminthes

Cited by 413 publications

References 33 publications

Back in time: a new systematic proposal for the Bilateria

Back in time: a new systematic proposal for the Bilateria

Assessing the root of bilaterian animals with scalable phylogenomic methods

Acoelomorpha: earliest branching bilaterians or deuterostomes?

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