development of radial and biradial symmetry: The evolution of bilaterality, The

American Zoologist, Sep 1998 by Martindale, Mark Q, Henry, Jonathan Q

A third scenario can also be considered (Fig. 5C). If a ctenophore-like organism represents the ancestor of both protostomes and deuterostomes, their descendants might have co-opted an existing axis (such as the anal axis) for constructing the dorsal-ventral axis. In this situation, asymmetric polarity along that axis would develop, possibly as the ancestors assumed a benthic existence, and descendent lines would have had to utilize one of the anal canals as their new mouth. Whether the anal pores of ctenophores represent the sites of either the protostome or deuterostome mouth remains to be seen.

There should be a way to determine whether the ctenophore anal axis (or other axes such as the tentacular or esophageal axes) represents an incipient dorsal-ventral axis. Recently, two sets of genes have been identified in fly and amphibian embryos which are causally involved in the establishment of the dorsal-ventral axis. One of these pairs of orthologous genes, the fly sog (short of gastrulation) and an ortholog in amphibians, chordin, have been shown to be functionally interchangeable with one another (Ferguson, 1996; DeRobertis and Sasai, 1996). sog is expressed in the ventral region of fly embryos, while its ortholog, chordin, is expressed in the dorsal region of amphibian embryos. When chordin is injected into fly embryos it promotes ventral fates, and when a modified sog is injected into frog embryos it promotes dorsal fates. The situation is identical, but complimentary, for the two genes decapentapalegic (dpp) from flies and Bone Morphogenic Protein-4 (BMP-4) from frogs. While dpp is expressed in the dorsal regions of the fly embryo, BMP-4 is expressed in the ventral regions of frog embryos. The most parsimonious interpretation of these results is that there has been a functional conservation in the molecular basis for dorsal-ventral polarity in protostome and deuterostome evolution. Care must be taken in the analysis of this signalling pathway, however, since antagonistic biochemical interactions such as these may have arisen numerous times evolutionarily to help establish or refine patterning events in different tissues and structures. The common protostome/deuterostome ancestor must have possessed orthologs of these genes, but it is not at all clear how they deploy these bilaterian molecular components of dorsalventral axis specification (Lowe and Wray, 1997). We are currently attempting to isolate these orthologs in both cnidarians and ctenophores to see whether bilaterian patterning genes have related roles in these diploblastic phyla. SUMMARY

While some aspects of early development are shared in the embryos of cnidarians and ctenophores, similarities are lost quickly after the first cleavage division. Ctenophores display a stereotyped cleavage program that generates cells in distinct positions with respect to other cells within the embryo and segregates developmental potential into defined lineages. Inductive ability is also redistributed into distinct cell lineages in ctenophore embryos and it is likely that the coordinated deployment of inducing activity, resulting in the formation of "organizing centers," may be one of the fundamental inventions of metazoan developmental programs that allowed for the establishment and exploitation of bilaterally symmetrical body plans (Fig. 2). The extent to which such changes in the early cleavage program have led to the radiation of diverse metazoan phyla exhibiting bilaterally symmetrical body plans, or whether these events are related to changes in life history stratagies, remains unclear. One way of understanding these changes is to learn more about the molecular basis of axis specification in the "Radiata," as virtually nothing is known about the evolution of the dorsal-ventral axis or the relationships between the oral-aboral or anterior-posterior axes in these animals. While we can speculate on these evolutionary events, the mechanistic basis for body plan evolution underlying the transition from radial to bilateral symmetry will be difficult to interpret until metazoan realationships are known.