Getting a head: Evidence for a conserved anterior head patterning gene network in arthropods

The head of chelicerates, such as spiders, scorpions and mites, is composed of the ocular, chelicerae and pedipalp segments and is considered to be homologous to the procephalon of insects which comprises the ocular, antennal and intercalary segments. Head segmentation in the spider, Parasteatoda tepidariorum, is a dynamic process in which a single stripe of expression of the P. tepidariorum hedgehog (hh) gene splits twice to form three separate stripes, which help pattern the three spider head segments. This dynamic hh stripe splitting process is dependent on spider homologues of the transcription factors orthodenticle (otd) and odd-paired (opa). Here we investigate the conservation of this dynamic patterning mechanism in two insect models: the hemimetabolous pea aphid, Acyrthosiphon pisum, and the holometabolous red flour beetle, Tribolium castaneum.. We show that insect hh, otd and opa homologues are expressed in a highly conserved temporal and spatial pattern during procephalon development in these insects. Our data are consistent with an ancestral insect state in which a single hh stripe splitting event underpins patterning of the ocular and antennal segments, followed by de novo formation of the intercalary hh stripe. Using parental RNAi in T. castaneum, we show that hh, otd and opa homologues exhibit striking similarities in their regulatory interactions during spider and insect head/procephalon segmentation. Our data suggest that hh, otd and opa homologues contribute to an ancient and largely conserved gene network controlling head/procephalon patterning in arthropods. We discuss the implications of these data for our understanding of the origin and evolution of the arthropod head, and propose a new model for the evolution of anterior patterning in holometabolous insects.