Acoelomorph flatworms and precambrian evolution

One of many open questions in evolution is the nature of bilaterian origins—when the first bilaterally symmetrical common ancestor (the Last Common Bilaterian, or LCB) to all of us mammals and insects and molluscs and polychaetes and so forth arose, and what it looked like. We know it had to have been small, soft, and wormlike, and that it lived over 600 million years ago, but unfortunately, it wasn't the kind of beast likely to be preserved in fossil deposits.

We do have a tool to help us get a glimpse of it, though: the analysis of extant organisms, searching for those common features that are likely to have been present in that first bilaterian; we're looking for the Last Common Bilaterian by finding the Least Common Denominators among living species. And one place to look is among the flatworms.

A recent paper by Bagun and Riutort examines one specific subgroup of the flatworms, the acoelomorphs (pronounced a-seel-o-morphs). These are tiny marine worms that have long been grouped under the platyhelminthes, but molecular work has been revealing that the platyhelminths have been a victim of our "worm is just a worm" bias, and are almost certainly polyphyletic. Bagun and Riutort argue that the acoels ought to be recognized as a separate phylum of their own, and further, that they represent basal bilaterians. They propose on the basis of molecular data that most of the Platyhelminthes belong in the protostome clade, and that they've secondarily lost characters common to most members of that group, such as segmentation. and that the acoelomorph flatworms are an early branch off the bilaterian root.

A new systematic and phylogenetic proposal for the Metazoa, based on molecular (18S+28S rDNA, Hox cluster genes and myosin II sequences, and let-7 gene expression data) and morphological characters. The Bilateria is divided into the Acoelomorpha (acoels+nemertodermatids), and the rest of the bilaterians, or Eubilateria, itself divided into the three big superclades: Deuterostomia, Ecdysozoa and Lophotrochozoa. The bulk of the Platyhelminthes is now within the Lophotrochozoa. The LCB and its descendants form the crown Bilateria reducing the extent of stem-group bilaterians. In turn, the LCE and its descendants (Deuterostomia, Ecdysozoa and Lophotrochozoa) form the crown Eubilateria. Note that the LCB for acoelomorphs eubilaterians is less complex than the LCE for Eubilateria. Bilaterian autapomorphies (black rectangles) are as follows: (1) bilateral symmetry, (2) two body axes (anteroposterior or AP, and dorsoventral, or DV), (3) endomesoderm, (4) anteriorly concentrated nervous system, and (5A) basic Hox cluster with four Hox genes and three ParaHox genes. The Eubilateria will have some autapomorphies that exclude the acoelomorphs: (5B), expanded Hox cluster gene (7 or 8 genes), (6) fully formed brain ganglia (with a neuropile), (7) through-gut (mouth anus), (8) excretory system, and (9) expression of the gene let-7. As suggested by some authors, other autapomorphies (white rectangles) of Eubilateria would be as follows: (10) coelomic cavities, and (11) segmentation. Characters 10 and 11 may had a monophyletic (10,11), a diphyletic (10',11' ) or a polyphyletic origin (not shown). If a deep position for the Platyhelminthes within the Lophotrochozoa is accepted, characters 7, 10, and 11 in Platyhelminthes reverted to a plesiomorphic condition (marked with an X). Synapomorphies uniting acoels and nemertodermatids into the Acoelomorpha are as follows: a, interconnecting ciliary root system, b, cilia with shaft-like transitions; c, duet spiral cleavage; and d, fine structure of frontal organs.

One reason this is important is that it changes our view of the earliest bilaterians. The cartoon below illustrates the point (with smily faces on critters!). Look at B first; this is one way we've been thinking about bilaterian evolution. An organism with radial symmetry, like a cnidarian polyp, acquired bilateral symmetry, and because modern deuterostomes and protostomes share complex characters like segmentation, anterior sensory structures, etc., the LCB had at least rudiments of that complexity. That's a substantial leap. Not for the organisms, of course…that didn't happen all at once, but the real problem is that the many intermediates left no trace and are invisible to us.

Figure A in the cartoon below shows the model that Bagun and Riutort are advancing: that there was a simpler LCB, and we can see its descendants in the acoelomorph flatworms.

Main scenarios (in a very simplified cheerful form) on the radial-bilaterian transition. A: The planuloid-acoeloid hypothesis. (1,2) It features a graded, step-by-step evolution of the Bilateria starting with a planuloid or planula-like organism from which derives a simple unsegmented and acoelomate acoeloid Last Common Bilaterian ancestor (LCB) similar to present-day acoel plathelminthes. From this ancestor derived the pseudocoelomate protostomates and, later on, protostomes and deuterostomes coelomates. B: The archicoelomate hypothesis. (7) See text for additional references. It features a swift transition from either a larval or an adult cnidarian to a complex or very complex LCB which already bears through-gut, eyes, coelom and, likely, segments and appendages. From this ancestor evolved the more complex protostomate and deuterostomates. In turn, acoelomate and pseudocoelomate unsegmented bilaterians derived at early and/or late stages of bilaterian evolution by morphological simplification from complex coelomate ancestors. A, anterior; AB, aboral; D, dorsal: O, oral; P, posterior; V, ventral.

Another useful part of their model is that they are arguing the LCB would have evolved from the planula larva of a cnidarian. Many radially symmetric cnidarians produce larvae that look like microscopic ciliated worms, such as the hydrozoan larva to the left. Now that is not such a large leap anymore, from an elongated planula to a gutless, blind, simple worm to a segmented worm. They also have a timeline based on the molecular data, suggesting that the transition from cnidarian to the LCB occurred 600-630 million years ago, that the transition from the LCB to the Eubilaterian occurred about 570 million years ago, and that the protostome-deuterostome split happened about 550 million years ago. I know the Intelligent Design gang looks at these numbers for pre-Cambrian and Cambrian events and thinks it means sudden appearance, but think about it: these transitions took place over thirty million years each. I always find it peculiar that people who find it reasonable to claim that life on earth has a history of only 6,000 years can simultaneously characterize events taking tens of millions of years and occurring half a billion years ago as abrupt.

On to some data…one particularly interesting part of this work is an examination of Hox gene distributions. The cnidarians typically only have two Hox genes. Most modern bilaterians have 7 or 8 or more Hox genes in a cluster, but the acoels have only 4 Hox paralogs, which are more similar to other bilaterian than cnidarian Hox genes, but are distinct in sequence from protostome (including platyhelminth) Hox genes. The diagram below shows our prior picture, in A, of the arrangement of genes in the Hox cluster, and how that maps onto a phylogenetic tree. B shows a similar tree, but with the new information from the Acoelomorpha added—they're intermediate between the Radiata and the Eubilateria.

Hox duplication evolution mapped onto a phylogenetic tree of Metazoan phyla which incorporates (tree in B) recent data on Hox and ParaHox gene clusters from acoelomorphs. A: Metazoan tree, circa 2000. Cnidarians have Hox and ParaHox genes representing only the most anterior (red) and posterior (blue) group Hox genes and its corresponding ParaHox genes (brown). All bilaterians have anterior (red), gene 3 (yellow), central (green), and posterior (blue) group Hox genes and anterior, gene 3, and posterior ParaHox genes (brown). Most gene groups, namely the central, duplicated extensively before the bilaterian radiation; therefore, the LCB did have a full complement of Hox genes. Note the big gap existing between cnidarians and all bilaterians. Broken lines indicates that colinearity has not yet been demonstrated. B: Resulting metazoan tree (circa 2004) which incorporates data from acoelomorphs. The LCB would have now a basic set of four Hox (anterior, gene 3, central and posterior) gene groups and, very likely, three ParaHox gene groups. The empty rectangle for anterior ParaHox in acoelomorphs indicates it has, so far, not been detected. At the base of the eubilaterian radiation (marked with an X), expansion of the Hox complex generated many of the central Hox genes. Additional genes duplicated within each bilaterian superclade, namely in the anterior and posterior gene groups. Note how the acoelomorph Hox/ParaHox gene cluster data fill the big gap between cnidarian and Eubilateria Hox/ParaHox gene clusters.

Bagun and Riutort also have a simple explanation for how the bilaterians could have evolved from the radiate cnidarians. Here's a cartoon of the morphological transition from a free-swimming cnidarian larva to a crawling bilaterian:

Planuloid-acoeloid scenarios at the radial-bilaterian transition. The ciliated planuloid (left) represents a mature organism bounded by a monolayered ectoderm (yellow) and bearing a condensed nerve net (blue), a tuft of cilia at the apical end (aboral, AB), and a blastoporal mouth/anus (red) at the basal end (oral, O). Chequered red/white indicates the solid endoderm/mesoendoderm. A: The evolutionary intermediate settles at the substratum along its O-AB axis, and evolves into a DV asymmetric acoeloid due to the forward movement (curved thin arrow) of the blastoporal mouth/anus to the ventral region. The brain is now at the anterior end from which several longitudinal nerve cords (thin blue lines) run ventrally (in protostomates) or dorsally (in deuterostomates) along the AP axis. Meanwhile, the mesodendoderm has sorted out into mesoderm (white spaces) and endoderm (red). B: The evolutionary intermediate settles on the blastopore down to the substratumand elongates by compressing the O-ABaxis (homologous to the DVaxis). A new AP axis is established by movement of the apical brain area forward (curved thin arrow). C: From6Aor 6B, the blastoporal mouth/anus elongates along the APaxis (middle, thin arrows) and seals centrally by amphistomy giving an organism with a through-gut (mouth and anus). D: A mature planuloid (left) derives by a paedomorphic mechanism (e.g. progenesis (15)) from an immature planula larva of a cnidarian with a similar life-cycle to extant cnidarians. From the planuloid, an acoeloid derives following either the scenario 6A or 6B. For other symbols, see legend of Fig. 1.

The model really only involves two innovations: retention of planuloid larval form in an adult, and a symmetry-breaking event that leads to the formation of a mouth. And it leads to some testable predictions about developmental genes in cnidarians and flatworms!

Assuming [the figure above] as the most-likely scenario, such symmetry breaking would represent the key event in the evolution of the Bilateria as it produced at once a third layer and a new orthogonal body axis (likely the DV) with its concurrent bilateral symmetry. Moreover, an anterior concentration of nerve cells was already in place. To diversify the expanded AP pattern a novel set of central Hox genes (see below) needed to be added between the anterior and posterior Hox genes already present in cnidarians. Such ideas could be tested by studying the expression of Hox/ParaHox and other anterior (e.g. orthodenticle, empty spiracles, distaless, Pax 6), posterior (caudal, Brachyury, forkhead, wingless), dorsal (decapentaplegic/Bone Morphogenetic Protein), ventral (short gastrultion/chordin), and mesoendodermal (snail, twist, GATA factors) genes in embryos and adults of selected acoelomorph species. Results could then be compared to the expression data that are accumulating fromplanula larvae and polyps of several species of cnidarians. Interestingly, an impressive number of these genes, namely expressed at posterior regions in bilaterians, is expressed in a radial manner around the blastoporal region in planulae. This supports the homology between the aboral-oral axis of cnidarians and the AP axis of bilaterians, oral in planula corresponding to posterior in bilaterians.

We're also getting an increasingly better focused image of what was going on in the pre-Cambrian and Cambrian. Funny, but it doesn't seem to involve any 'designers'.

Altogether, this reinforces the existence of a cryptic precambrian history of small, benthic, stem-group bilaterians, which left no trace fossils. The explosion of life forms during the Cambrian and thereafter would result from increasing body size and complexity linked to the emergence of indirectly developing larval forms in some lineages of stem deuterostomates, ecdysozoans and lophotrochozoans.

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