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

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

Of special interest is the diverse variation in symmetry seen in members of the Radiata. Both cnidarians and ctenophores now show various forms of symmetry in planes passing along the oral-aboral axis (Fig. 1). In some cnidarians, this takes the form of multiple planes of mirror symmetry, hence the moniker "radial symmetry". There is morphological evidence in some cnidarians that the number of planes of symmetry may be reduced, and that biradial (with two major planes of symmetry) or even bilateral body plans are present (with only one plane of mirror symmetry). For example, some hydrozoan medusae have scores of tentacles surrounding the margins of the bell, while other species have only two or four tentacles. Most adult anthozoans (e.g., corals and sea anemones) possess indicators of bilateral symmetry in the folded pleats of their gastrodermis. Recent evidence indicates that anthozoans are the basal members of the Cnidaria (Bridge et al., 1995; Odorico and Miller, 1997) and so it is possible that ancestral cnidarians were not radially symmetrical.

The symmetry properties displayed by ctenophores are significantly different from those of cnidarians and may represent an intermediate step in the evolution of bilaterality. Ctenophores have been described as being biradially symmetrical, with two perpendicular planes of symmetry (Fig. 1D) that run through the two tentacles (the tentacular plane) and the plane of the flattened esophagus (the "sagittal" plane) that define four body quadrants. The endodermally derived anal canals connect the gut to the external environment via the anal pores which are located at the aboral surface in two diametrically opposed quadrants (Fig. iD). Thus, the tentacular and sagittal planes of symmetry are not simple planes of mirror symmetry. Instead, these represent planes of two-fold mirror (rotational) symmetry. Thus, any plane that includes the oral-aboral axis represents a plane of rotational symmetry, including both the plane that passes through the anal pores and the plane orthogonal to it. In fact, ctenophores do not possess a single true plane of mirror symmetry. The diverse nature of symmetry properties amongst members of the Radiata raises several questions. Do their symmetry properties bear some relationship to those of bilaterians? Does the establishment of rotational symmetry have a different developmental/molecular basis than the establishment of mirror symmetry? For instance, the presence of diametrically distinct quadrants in ctenophores, which eliminates true radial symmetry, may represent precursors of secondary polarized axes, such as the dorsal-ventral axis of bilaterians. On the other hand, radial symmetry may represent a derived condition, and all eumetazoans may actually be constructed upon an underlying bilaterally symmetrical platform.

An understanding of the developmental basis of the symmetry properties in the Radiata is needed before any relationship to the evolution of bilaterian body plans can be obtained. This information will be difficult to interpret, however, since the phylogenetic relationships of these phyla to bilaterians, and to each other, have not yet been clarified. While cnidarians and ctenophores appear to occupy pivotal positions in metazoan phylogeny, there is no consensus as to their exact relationships to other extant phyla. Historically, ctenophores have been grouped with cnidarians as the Coelenterata (Christen et al., 1991; Morris, 1993) and compelling arguments have also been proposed which would either make the cnidarians the sister group to the bilaterians (Wainright et al., 1993) or position ctenophores as degenerate deuterostomes (Nielson, 1995). On the basis of developmental and morphological evidence, and for the sake of argument, we currently favor the view (Fig. 2) that ctenophores are the sister group to the Bilateria (Harbison, 1985; Ax, 1989; Schram, 1991; Eernisse et al., 1992). However, the next few years should bring us to a better understanding of early metazoan phylogeny.