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 [1-9]. 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 [6, 10]. Anterior Caudal repression in these species is achieved through unrelated translational repressors, the homeodomain protein Bicold [11] and the KH domain factor Mex-3 [6, 12], 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.