Comparison of early nerve cord development in insects and vertebrates

In recent years, evidence has accumulated that the insect ventral body side equals the dorsal side of the vertebrates and that chordates, during their evolution, have inverted their dorsoventral body axis (Arendt and Nübler-Jung, 1994, 1997; Holley et al., 1995; De Robertis and Sasai, 1996). In insects and vertebrates, the equivalent ‘neural’ body sides give rise to a prominent brain and nerve cord, and therefore the question whether insect and vertebrate centralized nervous systems (CNS) are homologous is again open for debate. In 1875, Anton Dohrn had proposed that vertebrates and arthropods have inherited their nerve cord from a common annelid-like ancestor (‘annelid theory’, Dohrn, 1875; reviewed in NüblerJung and Arendt, 1994). This is against the prevailing point of view that insect and vertebrate nerve cords evolved on opposite body sides of their last, very primitive common ancestor (‘Gastroneuralia-Notoneuralia concept’, Hatschek, 1888; Siewing, 1985; Ax, 1987; Brusca and Brusca, 1990; Gruner, 1993; Nielsen, 1995). A broad comparative analysis of the now available molecular and morphological data should help to resolve this issue. Ideally this analysis should involve – apart from insects and vertebrates – various additional phyla that are considered their closer relatives, such as crustaceans, annelids or enteropneusts, as well as other phyla that might serve as phylogenetic outgroups, such as nematodes and flatworms (for recent phylogenies, see e.g. Brusca and Brusca, 1990; Nielsen, 1995). We start here with a more limited approach, namely a comparison of nerve cord development in insects and vertebrates. The last two decades have seen enormous progress in the molecular and embryological analysis of neural development in selected insect and vertebrate species, and some striking similarities in brain and nerve cord development shared between insects and vertebrates have already been outlined (Holland et al., 1992; Thor, 1995; Arendt and NüblerJung, 1996; D’Alassio and Frasch, 1996; Weiss et al., 1998). The rapidly growing amount of data now allows considerable broadening of these comparisons to reveal additional similarities in unexpected detail. Homologous features of two given animal groups are those “that stem phylogenetically from the same feature.. in the immediate common ancestor of these organisms” (Ax, 1989; Bock, 1989) so that their “non-incidental resemblances are based on shared information” (Osche, 1973; see Schmitt, 1995). Evidently, it is important to add at which level of evolution any two features are supposed to be homologous (Bolker and Raff, 1996). For example, the various types of insect and vertebrate neurons will be homologous as neurons yet the question arises whether they are homologous also, for example, as motoneurons or as commissural interneurons. To 2309 Development 126, 2309-2325 (1999) Printed in Great Britain © The Company of Biologists Limited 1999 DEV9647