An ancient anterior patterning system promotes caudal repression and head formation in ecdysozoa

Posterior expression of Caudal is required for early embryonic development in nematodes, arthropods, and vertebrates. In Drosophila, ectopic Caudal in anterior cells can induce head defects, and in Caenorhabditis the absence of Caudal in anterior embryonic cells is required for proper development. Anterior Caudal repression in these species is achieved through unrelated translational repressors, the homeodomain protein Bicoid and the KH domain factor Mex-3, respectively. Here we report that the Mex-3 ortholog in the flour beetle Tribolium plays a crucial role in head formation and that Caudal in this species is repressed by the combined activities of Mex-3 and Zen-2, a protein sharing common ancestry with the dipteran morphogen Bicoid. We propose that Mex-3 represents an ancient "anterior" promoting factor common to all Ecdysozoa (and maybe all Bilateria), whose role has been usurped in higher dipterans by Bicoid.