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

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

If, on the other hand, the polarity of Hox gene expression is reversed, and "anterior" genes are expressed closer to the aboral sense organ (Fig. 4B), it would suggest that the mouth of radially/bilaterally symmetrical metazoans is homologous to the anus of bilaterians and that the mouth may have evolved in different locations in protostome and deuterostome lineages (see below). Of course, it is also possible that the anteriorposterior axis is not homologous with the oral-aboral axis. It could be, for example, that the oral-aboral axis corresponds more closely with the dorsal-ventral axis (Fig. 4C). For example, there are some derived ctenophores which have abandoned their pelagic existence and live on the sea floor. These "creeping" ctenophores lose their comb rows late in embryogenesis and move about with their mouth towards the substrate (i.e., "ventral") but with no preferred direction of movement, that is, no anteriorposterior polarity (G. Freeman, personal communication). In addition, it could be that the relationship of the oral-aboral axis is different between ctenophores and cnidarians, requiring that we completely reevaluate the phylogenetic relationship of these organisms to other extant metazoans (see Nielsen, 1995, for example). Finally, Hox genes may not be deployed in axis specification, but may be involved in cell type determination or other developmental functions (Davidson, 1991).

Lacalli (1996) has pointed out two possible scenarios for the evolution of the dorsal-ventral axis in bilaterians that also have implications for the formation of the anterior-posterior axis. In one scenario, an ancestor possessed a continuous digestive tract and dorsal-ventral polarity (as evidenced by the placement of the central nervous system and mouth on the ventral side). Deuterostomes, which utilize orthologous genes to establish the dorsal-ventral axis (see below), would have evolved by the formation of a new mouth, or through migration of the existing mouth to the ancestral "dorsal" side of the embryo (Fig. 5A). This scenario is complicated by the difficulty of envisioning transitional forms where the mouth attains the new position. Another scenario predicts that the common ancestor of both protostomes and deuterostomes possessed a blind gut and a dorsal-ventral axis. In this case, mouths would have evolved independently on different sides of the embryo with respect to the dorsal-ventral axis in protostome and deuterostome lines (Lacalli, 1996). If this scenario is true, it implies that there might have been an "inversion" of the anterior-posterior axis, where the mouth (the common mouth and anus) of the ancestor became the anus of bilaterians (Fig. 5B). The possible "inversion" of the oral-aboral axis points to the uncertainty in the evolutionary relationship of the body plans of radially and biradially symmetrical organisms to those of bilaterians. No good transitional organism extant, or fossilized, has yet been identified and the number of potential candidates, including the flatworms, appears to dwindle as the phylogenetic relationships of the Metazoa are unraveled (Aguinaldo et al., 1997; Balavoine, 1997; Valentine, 1997).