From Unity of Composition to Unity of Nervous Systems

Although Cuvier was considered to have won the 1830 debates, Geoffroy's philosophical anatomy remained remarkably influential during the subsequent decades. A resolution of the conflicting ideas was achieved, in part, by Darwin's evolutionary theory in which structural homology became an important criterion for establishing phylogenetic relationships. Moreover, with the advent of molecular developmental genetics, it has become clear that homology is a concept that applies not only to morphology, but also to genes and developmental processes. Indeed, and rather unexpectedly, more than 150 years after the famous debate, developmental genetics has provided experimental evidence for Geoffroy's unity of composition and specifically for his dorsoventral axis inversion hypothesis that appeared to be so convincingly refuted by Cuvier.

The discovery that a common developmental genetic program underlies dorsoventral axis formation in both insects and vertebrates was based on the analysis of two sets of homologous genes that encode morphogens in the model systems Drosophila and Xenopus (Holley et al., 1995; Schmidt et al., 1995; De Robertis and Sassai, 1996; Holley and Ferguson, 1997). The transforming growth factor b (TGFb) family member encoded by the decapentaplegic (dpp) gene is expressed dor-sally and promotes dorsal fate in Drosophila, whereas its vertebrate orthologue Bone morphoge-netic protein (Bmp4) is expressed ventrally and promotes ventral fate in Xenopus. These morphogens are antagonized by the secreted products of the orthologous genes short gastrulation (sog) in Drosophila and Chordin in Xenopus. Importantly, the site of action where sog/Chordin expression inhibits dpp/Bmp4 signaling corresponds in both insects and vertebrates to the region of the dorso-ventral body axis that gives rise to the embryonic neuroectoderm from which the nervous system derives (see below).

These results provide strong evidence that the molecular interactions that occur on the ventral side of insects are homologous (in Geoffroy's sense, analogous) to those that occur on the dorsal side of vertebrates - an observation that revitalizes Geoffroy's initial proposition of the unity of composition between arthropods and mammals and supports the hypothesis of a dorsoventral inversion of their body axes during the course of evolution (Arendt and NĂ¼bler-Jung, 1994). Moreover, these results also provide strong evidence that the molecular interactions that lead to the formation of the ventral CNS in insects are homologous to those that lead to the formation of the dorsal CNS in vertebrates, indicating a dorsoventral body axis inversion as the most parsimonious explanation for the dor-soventrally inverted topology of the CNS that characterizes Gastroneuralia versus Notoneuralia.

Comparable molecular genetic studies on other sets of homologous genes in various model systems ranging from annelids and arthropods to mammals are providing further evidence that Geoffroy's unity of composition might be the result of a developmental construction plan that is shared by all bilaterian animals. Thus, evolutionarily conserved developmental control genes act not only in dorsoventral axis specification but also in anteroposterior axis formation, segmentation, neurogenesis, axogenesis, and eye/photoreceptor cell development through comparable molecular mechanisms that appear to be conserved throughout most of the animal kingdom. The implications of these findings are far-reaching. They suggest that, although diverse in their mode of development and adult morphology, bilateral animals derived by descent from a common ancestor, the Urbilateria, which may already have evolved a rather complex body plan (De Robertis and Sasai, 1996). Accordingly, the urbilaterian nervous system may already have evolved structural features that prefigured elements of the nervous systems of the descendent bilaterian animals. If this were indeed the case, then the ventrally located arthropod nervous system may be homologous to the dorsally located chordate nervous system; the insect brain may be composed of structural units homologous to those of the vertebrate brain; the visual system of a fly may be homologous to the visual system of a mammal. The plausibility of this scenario is particularly evident with regard to the conserved mechanisms of anteroposterior and dor-soventral patterning of the nervous system that operate in insects and vertebrates.

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