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

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

Ctenophores are composed of four nearly identical quadrants separated by the tentacular and esophageal (sagittal) planes (Fig. 2D). Each of these planes would define planes of mirror symmetry were it not for the presence of the anal canals. Cell lineage studies have shown that each of the four quadrants normally contributes to structures along both the tentacular and esophageal axes. For example, each of the first four cells gives rise to portions of one of the tentacular apparati. This situation is not true for the formation of the anal canals. Cell lineage analysis in the lobate ctenophore Mnemiopsis leidyi has revealed a phenomenon that we refer to as "diagonal determination" (Martindale and Henry, 1995). The two endodermally-derived anal canals are generated from descendants of diagonally opposed 2M macromeres at the 60 cell-stage (the backslash or "\" pair). The other two 2M macromeres (the slash or "/" pair) do not contribute to the formation of anal canals, but they do make circumesophageal and longitudinal muscle cells, which are not produced by the "\" lineages. Thus, these four seemingly identical 2M macromeres, which are all in contact with one another at the animal (oral) pole, are differentially organized as two pairs of diagonally opposed cells (Fig. 3). In fact, these quadrant specific differences are established at the four-cell stage.

Depending on whether radial or bilateral symmetry is ancestral, the anal axis of ctenophores could represent an incipient precursor, or a remnant, of the dorsal-ventral axis found in bilaterians. Does the formation of the anal axis in ctenophores tell us anything about how bilateral symmetry arose in metazoan evolution? Our ability to obtain answers to these questions is hampered by the fact that we do yet not understand the relationships of the major body axes of the radiata to those of the bilaterians. It is often assumed that the major longitudinal axis of the Radiata (oral-aboral axis) is homologous to the anterior-posterior axis of bilaterians. However, there is no compelling evidence to support this claim, and even if it holds, it remains unclear which end of the oral-aboral axis corresponds to the anterior pole in bilaterians. This question has become all the more interesting and tractable due to recent work showing a conserved molecular basis for the formation of both the anterior-posterior and dorsal-ventral axes in bilaterians.

Several interesting implications arise when one considers the possible evolutionary transitions between radial and bilateral symmetry. Highly conserved and robust molecular markers currently exist for both the anterior-posterior (Slack et al., 1993; Akam, 1995) and dorsal-ventral axes (Ferguson, 1996; DeRobertis and Sasai, 1996) in all bilaterians thus examined, and it is likely that these genes are also expressed in radially and biradially symmetrical metazoans. The markers for the anterior-posterior axis are the Hox genes. Hox genes have been reported in both cnidarians (Schierwater et aL, 1991; Schummer et al., 1992; Naito et al., 1993; Shenk et aL, 1993a, b. Finnerty and Martindale, 1997) and ctenophores (Finnerty et al., 1996); however their patterns of expression have yet to be thoroughly explored in either group. A comparison of Hox gene expression in the Radiata might reveal the actual relationship of the longitudinal axes in these two groups. For example, if "anterior" Hox genes (such as a labial ortholog) are expressed closer to the mouth than "midbody" or "posterior" Hox genes, it would provide evidence that not only are the oralaboral axis and the anterior-posterior axis homologous, but that the polarity along these axes has been conserved (Fig. 4A). The fact that adult ctenophores swim with their mouth forward, they possess anal canals on the side opposite the mouth, and the oral pole is derived from the "animal" pole of the embryo (as defined by the first cleavage division) suggests that the oral pole in ctenophores corresponds to the anterior pole of bilaterian descendants.