Back in time: a new systematic proposal for the Bilateria

Abstract

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.

Figure 1

Coincident changes in the branch leading to the LCBA node under (a) the complex Urbilateria hypothesis (archicoelomate theory; Remane 1963; Kimmell 1996; Adoutte et al. 2000) and (b) the simple Urbilateria hypothesis (planuloid–acoeloid theory; Hyman 1951; Salvini-Plawen 1978). Note that in the complex Urbilateria scenario, characters (a–k) clump at the LCBA node that by definition corresponds to the last common ancestor of protostomes and deuterostomes (P/D LCA). Under the simple Urbilateria hypothesis, new clades intercalate and separate the LCBA from the P/D LCA helping to distribute character changes (a–m) across a series of stem branches and to polarize them. Under this scenario, the LCBA is morphologically simpler than the P/D LCA. Note that characters j and k could be either monophyletic (j,k) or di- or polyphyletic (j′, j″, k′, k″). l and m represent protostome- and deuterostome-specific characters. Grey ovals indicate the stem branches where key innovations (new characters) appeared.

Figure 2

Bayesian analysis of 18S+28S sequences (3696 nts) from 106 metazoan representatives with Cnidaria as the outgroup. Posterior probabilities are indicated when less than 100%, otherwise a bullet is present on the node. Phyla are collapsed and numbers in parentheses indicate the number of taxa sampled if more than one. The monophyly of each phylum has maximum support (except for gastrotrichs). Boxed groups correspond to long-branched or problematic groups for which specific analyses were carried out (see electronic supplementary material). The scale bar indicates the number of changes per site.

Figure 3

Bayesian analysis of concatenated sequences for 18S, 28S and 11 nuclear protein genes (9290 nts) from 74 metazoan representatives with Cnidaria as the outgroup. Posterior probabilities are indicated when less than 100%, otherwise a bullet is present on the node. Phyla are collapsed and numbers in parentheses indicate the number of taxa sampled if more than one. The monophyly of each phylum has maximum support. The scale bar indicates the number of changes per site. For further details, see electronic supplementary material.

Figure 4

A new systematic proposal for the Bilateria. Morphological and molecular characters (HOX cluster genes and microRNA sets) have been mapped onto a backbone tree drawn from 18S+28S rDNA and 11 nuclear genes. The new Bilateria includes the Cnidaria and the former Bilateria, now dubbed as Triploblastica, the latter split into a paraphyletic ‘Acoelomorpha’ (Acoela and Nemertodermatida) and the rest of the bilaterians or Nephrozoa. Note that the LCBA for cnidarians+Triploblastica is less complex than the ancestor for Triploblastica. Bilaterian autapomorphies (vertical solid lines and empty and hatched inverted triangles) are as follows: 1, D–V axis; 2, bilateral symmetry; 3, HOX/ParaHOX clusters (3A: 2 HOX/2 ParaHOX); 4, microRNA sets (4A: basic bilaterian set). The Triploblastica have some autapomorphies that exclude cnidarians: 3B (4 Hox/3 ParaHox); 4B, a miRNA set of five out of six genes; 5, mesoderm; 6, clustered nerve cells at the anterior end. Finally, the Nephrozoa (=Protostomes+Deuterostomes at the P/D LCA node) will have some autapomorphies that exclude acoelomorphs: 3C, an expanded HOX cluster gene of seven to eight genes; 4C, a nephrozoan miRNA set of 20 or more genes; 7, small anterior brain ganglia and ventral nerve cords; 8, through gut (mouth+anus); 9, excretory system (=protonephridia). As suggested by some authors, other autapomorphies of Nephrozoa would be: 10, coelomic cavities; 11, body segmentation, though they may have a monophyletic or a polyphyletic origin. Some autapomorphies for the Deuterostomia, Lophotrochozoa and Ecdysozoa are indicated: 4D–4G, specific miRNA sets; 12, post-anal tail; 13, gill slits; 14, ecdysis. x, y (broken lines), postulated synapomorphies for a monophyletic Acoelomorpha (Smith et al. 1986). x, special structure of the basal body-rootlet system complex and the ciliary tips; y, fine structure of the frontal organ. Grey ovals indicate the stem branches where key innovations appeared. See text for further details and main references.