The genome sequences of two non-bilaterian animals, the cnidarians Nematostella vectensis and Hydra magnipapillata, have been recently completed. These new data lead to the fascinating result that the complement of Hox genes in the cnidarian ancestor is considerably lower than that in the bilaterians, although the complexity of their genome is otherwise similar (Technau et al. 2005). Thus, there is a correlation between the radiation of the Bilateria and the expansion of the Hox complex.

In the first part of this chapter, we shall present and discuss these data. In the second part, we shall present a novel hypothesis accounting for this phenomenon. In short, we surmise that the expansion of the Hox complex at the base of the Bilateria was due to a series of transposition events. Indeed, we hypothesise that the Hox genes themselves originate from transposons. The main support for this hypothesis is provided by the similarity between the homeodomain and the DNA-binding domain of bacterial integrases and eukaryotic transposases. We also examine some very precise rearrangements of the Hox complex in the Drosophilidae lineage. In the third part, we propose a scenario for the evolution of the Hox complex from the basic complement of Hox genes in the common ancestor of cnidarian and bilaterian animals. This scenario, based on our transposition hypothesis, accounts for several properties of the extant Hox genes.

TO SET THE SCENE: THE HOX EXPLOSION

The homeobox is a conserved motif found in a huge variety of eukaryotic genes, encoding a DNA-binding domain.