Comparative analysis of Wingless patterning in the embryonic grasshopper eye

The signaling factor Wingless regulates multiple steps during the postembryonic development of the Drosophila eye. To obtain insight into the molecular regulation of embryonic eye development in primitive insects, we studied the expression of wg and genes projected to interact with wg in the grasshopper Schistocerca americana. We find that the dynamic and complex expression of wg in the early grasshopper procephalon results in three paired expression domains with relevance to eye primordium development. By comparison with Drosophila, these domains are compatible with a conserved function of wg during anteroposterior and dorsoventral axis formation by repression of retinal differentiation and stimulation of tissue proliferation. This is further supported by the expression of grasshopper orthologs of the retina determination genes sine oculis and eyes absent, and by inhibition of retina differentiation in grasshopper eye primordia cultured with LiCl. Surprisingly, the expression of wg and the grasshopper orthologs of pannier, fringe, Delta, and Iroquois complex is inconsistent with induction of midline centered Notch signaling activity, which is essential for Drosophila retina development. Similarly substantial evolutionary divergence is found concerning the control of retina versus head epidermis specification. The transcription factor Extradenticle (Exd), which cooperates with wg in specifying the Drosophila head epidermis, is not detected outside the labral and antennal primordia in the embryonic grasshopper head. Our results, which provide the first insight into the molecular control of eye primordium formation in primitive insects, suggest substantial modification of this process during the evolution of the Drosophila mode of postembryonic eye development.