Anteroposterior patterning of Drosophila ocelli requires an anti-repressor mechanism within the hh pathway mediated by the Six3 gene Optix

In addition to compound eyes, most insects possess a set of three dorsal ocelli that develop at the vertices of a triangular cuticle patch, forming the ocellar complex. The wingless and hedgehog signaling pathways, together with the transcription factor encoded by orthodenticle, are known to play major roles in the specification and patterning of the ocellar complex. Specifically, hedgehog is responsible for the choice between ocellus and cuticle fates within the ocellar complex primordium. However, the interactions between signals and transcription factors known to date do not fully explain how this choice is controlled. We show that this binary choice depends on dynamic changes in the domains of hedgehog signaling. In this dynamics, the restricted expression of engrailed, a hedgehog signaling target, is key because it defines a domain within the complex where hedgehog transcription is maintained while the pathway activity is blocked. We further show that the Drosophila Six3, optix, is expressed in and required for the development of the anterior ocellus specifically, limiting the ocellar expression domain of en. This finding confirms previous genetic evidence that the spatial allocation of the primordia of anterior and posterior ocelli is differentially regulated, which may apply to the patterning of the insect head in general.