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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Basic embryology

In the great majority of the living, bilaterally symmetrical animals, the blastulae have an animal-vegetal polarity. Generally, the animal pole corresponds to the pole where the polar bodies are formed. The cells of the animal hemisphere form the outer epithelial covering of the future adult (cf. Henry et al., 2001), whereas the cells of the opposite vegetal hemisphere contribute to the development of the central gut tube and the mesoderm.

During gastrulation the cells around the vegetal pole move inside the embryo. Irrespective of the way in which gastrulation occurs, gastrulation itself is common to almost all animals. Thus, it can be assumed that evolution in the embryos of the ancestors of the bilaterians resulted in a process of gastrulation that changed a bipolar blastula (Fig. 1A) into a bipolar gastrula (Fig. 1B) with one opening, the blastopore, at the vegetal pole. This blastopore opening persists and can function either in the formation of the mouth, the anus, or both, or neither.


Fig. 1. Median sections of gastrulae in amphioxus; sections are oriented with anterior-posterior axis from left to right anad the doro-ventral axis from top to bottom. A. Young gastrula with initiation of blastopore formation beginning. B. advanced gastrula with posterior blastopore that will become the anus. Note the position of neurogenic ectoderm at the dorsal blastopore lip near the presumptive chorda-mesoderm. (Modified from Nelsen, 1953).

In the Deuterostomata, the blastopore is formed at the vegetal (posterior) pole of the embryo (Fig. 1A) and is transformed into the anus (Fig. 1B) (cf. Tagawa et al., 2001). In deuterostomes, a mouth opening has to be formed secondarily towards the anterior end of the embryo. In protostomes on the other hand, the initially posterior blastopore (Fig. 2B) eventually becomes the anterior mouth opening (Fig. 3C) due to rotation from the posterior end of the embryo to an anterior-ventral position.


Fig. 2. Blastula of 32-cell stage in Patella vulgata prior to the initiation of gastrulation. A. vegetal view. B. median-section of same as indicated in A. (Modified from van den Biggelaar, 1977; van den Biggelaar and Guerrier, 1979).

One way to achieve this rotation involves a complex series of cell movements (Damen and Dictus, 1997). The spatial dynamics of blastopore cell lineages over the course of gastrulation are such that at least in spiralians there is an internalization of B-quadrant midline lineages and a corresponding external migration of the D-quadrant midline lineages to spatially replace them. The more lateral A- and C-quadrant lineages of the blastopore lip pull away, migrate dorsally to occupy what had been the D-quadrant midline.

The specifics of these migrations involve several steps and can be clearly seen in Patella (Damen, 1994). First, derivations of cell 2d grow posteriorly and ventrally from their original position on the dorsal side of the embryo (Fig. 3A, C). Second, derivatives of cells 2b (in part), 3a, and 3b move internally (Figs. 2B, 3C), and another part of the 2b lineage moves laterally and dorsally (Figs. 2B, 3). Third, the derivatives of the macromeres move internally (Figs. 2, 3C). Thus, the ventral midline itself of spiralians, which separates the stomodeum and anus, is derived specifically from the 2d lineage, located initially at the embryonic dorsal, D-quadrant, midline of the blastopore lip. As a result of these movements, the blastopore comes to attain an anterior ventral position. Examination of published cell lineage work across the Spiralia (cf. Wilson, 1892; Åkesson, 1967; Anderson, 1966) reveals that morphogenetic transformations are a general feature of spiralian development. In most cases, this results in a bending of the animal-vegetal axis by some 90 degrees, as the vegetal blastopore migrates to an antero-ventral position along the B-quadrant midline. In embryos of the oligochaete Tubifex (Penners 1922, 1924; Shimizu, 1982) and of the leeches Helobdella and Theremyzon (Stent, 1999) the cells of the ventral nerve cord are also derived from the originally dorsal cell 2d.


Fig. 3. Schematic drawings of post gastrulation, 24-28 hour trochophore larva of Patella vulgata. Cell lineages marked. Note that the progeny of cell 2d, which has a dorsal position in the 32-cell stage as shown in Fig. 2, has attained a ventral position in the larva. A. ventral view. B. dorsal view. C. median-section deduced from A and B. (A and B modified from Damen and Dictus, 1997).