Contributions to Zoology, 71 (1/3) (2002)J.A.M. van den Biggelaar; E. Edsinger-Gonzales; F.R. Schram: The improbability of dorso-ventral axis inversion during animal evolution, as presumed by Geoffroy Saint Hilaire

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Amphistomy

In the above discussion, amphistomy as an alternative method for the development of two openings during gastrulation has not yet been considered (Fig. 5). In this particular mode of gastrulation, extension of the cells on the “dorsal” side of the early gastrula relocates the blastopore to a “ventral” position. The lateral lips are then said to fuse leaving two openings: an anterior aperture that will become the mouth, and a posterior opening that will become anus. Under this scenario, the blastopore develops into both anal and mouth openings. Such amphistomy is an integral feature of the Trochea Theory (Nielsen, 2001; Nielsen & Nørrevang, 1985), and is often invoked in molecular considerations of axis inversion (Arendt and Nübler-Jung, 1997). The idea of fusion of the lateral lips of the blastopore, and the formation of the ventral midline by the fused lateral lips, as described by Nielsen (2001) originated from descriptions of the early development of an annelid, Polygordius (Woltereck, 1904), an onychophoran, Peripatopsis (Manton, 1949), a nematode, Pontonema (Malakhov, 1994), and an arthropod, Lucilia (Davis, 1967). Lartillot et al. (2002) also assume an amphistomous gastrulation in the mollusc Patella. We suggest that the amphistomy hypothesis mistakenly derives the protostome ventral midline from cell lineages forming lips of the blastopore at the onset of gastrulation.

FIG2

Fig. 5. Amphistomy. A. sequence of stages of the annelid, Polygordius sp., note that posterior aspect of blastopore closes, only anterior part develops into mouth. (Modified from Nielsen, 2001). B. sequence of stages of Peripatopsis moseleyi, note that as blastopore closes, a separate stomoproctodeal slit opens anteriorly (Modified from Manton, 1949). C. sequence of stages in cell lineage migration leading up to gastrulation in Caenorhabditis elegans (Modified from Schierenberg, 1997).

What occurs in annelids? In Polygordius, according to Woltereck (1904), the four cells of the fourth quartet of micromeres 4a-4d have a position at the blastopore. The lateral micromeres 4a and 4c grow towards each other (Fig. 5A), by which means the blastopore achieves the form of an hourglass. After both cells have come to touch each other, the blastopore is effectively divided into two openings. The anterior opening becomes the prostoma, which will persist as the mouth opening to the separately developing midgut. Then, curiously enough, Woltereck explicitly states that the posterior opening does not become the anus! Rather, that part of the blastopore opening closes within a short time (Fig. 5A). Only later on does the actual anal opening appear amongst derivatives of cell 2d. This process completely corresponds with that described above for Patella. Instead of giving rise to mouth and anus, the blastopore of Polygordius only develops the mouth, and the ventral midline is developed from derivatives of cell 2d that had an original dorsal position at the blastula stage.

What happens in the onychophorans? Manton (1949) carried on an extensive study of embryology in Peripatopsis. The blastopore develops on the germinal disc and out from this opening, cells proliferate beneath the ectoderm to form the endoderm (Fig. 5B). This opening then begins to shrink, or is closed, and a separate, slightly more anterior opening appears later during development, the stomo-proctodeal slit. This in turn elongates along an anterior posterior axis while the lateral lips converge and fuse leaving an anterior stomodeal and posterior proctodeal opening. There is no hard evidence that these two openings correspond with the anterior and posterior openings of the former blastopore. This indeed is a situation that is mirrored in a great number of arthropods (cf. Anderson, 1973).

What happens in nematodes? If we take Caenorhabditis as an example (Schierenberg, 1997), it appears that prior to gastrulation the C cell has a postero-dorsal and the D cell a posterior position (Fig. 5C). During gastrulation the D lineage moves antero-ventrally whereas part of the C progeny move to the posterior pole and then continue in antero-ventral direction. So, also in a nematode one can observe that cells with an original exclusively dorsal position prior to gastrulation later can be found at the ventral side.

Collectively, and despite potential differences in the ultimate fate of the blastopore in different protostome lineages, a closer examination of morphogenesis in protostomes reveals that the ventral midline of the adult is derived from cells with an initially dorsal or dorso-lateral position. Thus the inversion of the dorsal-ventral axis in adult bilaterians can be attributed to differences in morphogenetic transformation of embryo to adult.