Figure 1 Morphogenesis of the ventral nerve cord in a prototype insect (a) and of the dorsal neural tube in a prototype vertebrate (b). Arrows indicate ontogenetic sequences; yellow-green, neurogenic ectoderm; blue, epidermal ectoderm. Reproduced from Arendt, D. and Nubler-Jung, K. 1999. Comparison of early nerve cord development in insects and vertebrates. Development 126, 2309-2325, with permission from The Company of Biologists Ltd.
However, starting in the 1980s, a number of key findings resulting from developmental biological analyses of animal body axis formation began to call into question the validity of the Gastroneuralia/ Notoneuralia subdivision and, in doing so, provided initial support for the idea of a monophyletic origin of the bilaterian nervous system. In a nutshell, these findings demonstrated that the molecular genetic mechanisms of anteroposterior axis formation are shared among all bilaterians and that the molecular genetic mechanisms of dorsoventral axis formation in vertebrates are similar to those that operate in insects, only that their dorsoventral topology is inverted, upside-down. If dorsal in vertebrates corresponds to ventral in insects, might not the dorsal nerve cord of Notoneuralia in fact correspond to the ventral nerve cord of Gastroneuralia?
This axial inversion hypothesis was remarkable not only because it was based on unequivocal molecular genetic evidence, but also because it provided support for an old and much-derided view that emerged in the early nineteenth century. Its first proponent was the French zoologist Geoffroy Saint-Hilaire, in opposition to his countryman, the comparative anatomist Cuvier. Both engaged in a debate about a fundamental issue in the biological sciences, namely, whether animal structure ought to be explained primarily by reference to function or rather by morphological laws. At the heart of this debate was the question of whether a common structural plan, or Bauplan, underlies all animal development, thus indicating homology of structures across different animal phyla. Contemporary developmental biological studies based on analyses of expression and function of homologous regulatory control genes in various animal model systems have revived this fundamental question and contributed novel insight into the issue of homology of nervous systems. In this article, we will begin with this famous debate, consider the impact of molecular developmental genetics on a bilaterian nervous system Bauplan, and then discuss the current data for and against a common evolutionary origin of the nervous system. Though our main emphasis will be on conserved mechanisms of anteroposterior and dorsoventral patterning of the nervous system in insect and vertebrate model systems, we will also consider gene expression studies in invertebrates such as hemichordates and cnidarians.
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