Evolution of the insect terminal patterning system—Insights from the milkweed bug, Oncopeltus fasciatus

Abstract The anterior and posterior ends of the insect embryo are patterned through the terminal patterning system, which is best known from the fruitfly Drosophila melanogaster . In Drosophila, the RTK receptor Torso and its presumed co-activator Torso-like initiate a signaling cascade, which activates two terminal gap genes, tailless and huckebein . These in turn interact with various patterning genes to define terminal structures. Work on other insect species has shown that this system is poorly conserved, and not all of its components have been found in all cases studied. We place the variability of the system within a broader phylogenetic framework. We describe the expression and knock-down phenotypes of the homologues of terminal patterning genes in the hemimetabolous Oncopeltus fasciatus . We have examined the interactions among these genes and between them and other patterning genes. We demonstrate that all of these genes have different roles in Oncopeltus relative to Drosophila ; torso-like is expressed in follicle cells during oogenesis and is involved in the invagination of the blastoderm to form the germ band, and possibly also in defining the growth zone; tailless is regulated by orthodenticle and has a role only in anterior determination; huckebein is expressed only in the middle of the blastoderm; finally, torso was not found in Oncopeltus and its role in terminal patterning seems novel within holometabolous insects. We then use our data, together with published data on other insects, to reconstruct the evolution of the terminal patterning gene network in insects. We suggest that the Drosophila terminal patterning network evolved recently in the lineage leading to the Diptera, and represents an example of evolutionary “tinkering”, where pre-existing pathways are co-opted for a new function.