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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A broader perspective

The evolution of highly divergent adult body plans across the Eumetazoa is the great, unsolved mystery in the diversification of life. Fundamental to this is the homology and evolution of the adult axes between animal body plans. The developmental expression and function of homologous genes in distantly related taxa has suggested a previously unrecognized level of homology between otherwise highly disparate axes and body plans. For instance, there is increasing evidence for the conserved utilization of Hox genes in patterning the primary adult body axis across eumetazoans (Gauchat, et al., 2000). Within the Bilateria there is the now well-recognized conservation but presumed inversion of the sog/chordindpp/bmp-4 gene network in patterning the neural midline or dorsal-ventral axis of protostomes versus deuterostomes (Wilkins, 2002), and this neural genetic network has been used to resurrect the idea of a protostome-deuterostome dorso-ventral axis inversion. However, from a comparative perspective, the topological inversion of axial-defining structures between taxa, such as the ventral versus dorsal nerve cords of protostomes versus deuterostomes, has lead to circular arguments concerning axial homology and ancestry between disparate body plans.

Nevertheless, we firmly believe that extreme caution is called for in considering such radical hypotheses. The proponents of axis inversion based on expressions of developmental genes have divorced issues of developmental genetics from critical embryological cell lineage work. Perhaps in part it is a manifestation of the phenomenon of the “cutting edge,” where “new and modern” research in development gets carried away in its enthusiasm to supplant “old and staid” studies of embryology. Whatever the reason, modern proponents of axis inversion have repeated the mistake of Geoffroy Saint-Hilaire: too much attention is paid to later phases of development at the expense of ignoring information from the earliest stages of ontogeny.

Though the conservation of developmental genes is indeed particularly striking, given the diversity and dissimilarities of bilaterian body plans, interpretation of these expression patterns requires that they be tempered within an operant framework of multiple alternative hypotheses. Inversion, while attractive in its simplicity and compelling in regards to its historical roots, is only one possibility. Cell lineage studies of earliest embryonic stages suggests that migrations and topological rotation of micromere derivatives cannot be ignored as an alternative explanation for dichotomous patterns of gene expression.

We must keep in mind that our knowledge of cell lineages is based on relatively few animals, and our examination of patterns of expression of developmental genes has focused on even fewer model systems. In evaluating alternative hypotheses, it will be absolutely necessary to expand the knowledge base with more comprehensive taxonomic sampling in studies of both early ontogeny as well as gene expression.