Evolution of the bilaterian body axes

Most of the more than 30 body plans of the now living phyla of multicellular animals (metazoa) share bilateral body symmetry and they likely evolved within a short period of time in the later Neoproterozoic and early Cambrian roughly 600 million years ago. No new major metazoan body plan arose thereafter. Members of only four to five metazoan taxa show simpler, in many cases radially symmetrical body organisation. It is generally assumed that the first bilaterians originated from radially symmetric ancestors. This transition is one of the most important and enigmatic events in animal phylogeny, as the elaboration of bilateral body symmetry is correlated with the invention of several key features of higher animals, i.e. a third mesodermal germ layer, cephalization, and a centralized nervous system. The recent characterization of a comprehensive set of developmental genes involved in establishing axial polarity in the embryos of both radially and bilaterally symmetric metazoans strongly supports a view that the two orthogonal bilaterian body axes (anterior-posterior and dorsal-ventral) are related to an ancestral oral-aboral body axis. The rationale in this proposal is to investigate two of the major cell signalling systems involved in metazoan axis formation - canonical Wnt signalling and Bmp-Chordin signalling - in Isodiametra pulchra and Macrostomum lignano, acoel and rhabditophoran Platyhelminthes regarded to represent two of the most basal groups of extant bilaterians. We expect that these studies will contribute to an understanding of how bilaterally symmetrical body plans arose from simpler ancestral forms.

Most of the more than 30 body plans of the now living phyla of multicellular animals (metazoa) share bilateral body symmetry defined by two body axes, anterior-posterior and dorsal-ventral. They evolved within a short period of time roughly 600 million years ago. Members of only four to five metazoan taxa including cnidarians show simpler, in many cases radially symmetrical body organisation with only one oral-aboral body axis. It is generally assumed that the first bilaterians originated from radially symmetric ancestors. This transition is one of the most important and enigmatic events in animal phylogeny. A set of conserved signaling pathways controls axis formation during early embryogenesis. We investigate these pathways in ancestral animal groups to gain molecular insight in the relationships between the two bilaterian body axes and the more ancestral cnidarian body axis. In this research proposal, we used genetic databases from two basal bilaterian flatworms, Macrostomum lignano und Isodiametra pulchra, to characterize Wnt signaling genes. Isodiametra is of particular interest, as it may belong to the most ancestral bilaterian phylum. We therefore characterized in detail its life cycle and its sexual reproduction under laboratory culture conditions. For both worms, we found a large set of wnt genes, which we will continue to study. We were also able to show that alsterpaullone, a pharmacological inhibitor know to activate Wnt signalling, activates posterior fate in Isodiametra and suppresses the formation of anterior structures. This is consistent with a known posterior function of Wnt signaling in other bilaterian phyla. Our main result is the characterization of sFRP genes in Macrostomum and Isodiametra as well as in the cnidarians Hydra and Nematostella. sFRP genes encode secreted factors known to act as Wnt inhibitors. In both cnidarians, an sFRP gene plays a central role in aboral development, while oral fate is regulated by Wnt factors. Based on our data and data in the recent literature we propose that the Wnt-sFRP complex represents the ancestral mode to pattern the primary body axis in early radially symmetric eumetazoans, and that bilaterians have inherited this complex to pattern their anterior-posterior axis. This would relate for the first time by a clear molecular complex the ancestral oral-aboral with the bilaterian anterior-posterior body axis. The anterior end in bilaterians would correspond to the aboral pole in cnidarians, the posterior end to the oral pole. Our results on the expression of a Macrostomum sFRP gene during anterior neuronal development are consistent with this view.