Sex-specific gene interactions in the patterning of Oncopeltus fasciatus genitalia

Genitalia play an important role in the life histories of insects, as in other animals. These structures are a unique developmental system to explore as they are rapidly evolving sexually dimorphic structures derived from multiple segment primordia. Despite the importance of insect genitalia, descriptions of their genetic patterning have been limited to fruit flies. In this study, we report the functions, interactions and regulation of appendage patterning genes (e.g. homothorax, dachshund, and Distal-less) in the milkweed bug Oncopeltus fasciatus. Female O. fasciatus have a multi-jointed ovipositor while male O. fasciatus have a genital capsule consisting of large gonocoxopodites and claspers. O. fasciatus required appendage-patterning genes for development of the male claspers, but not the proximal gonocoxopodite, suggesting a non-appendicular origin for this structure. The posterior Hox genes (abdominal-A and Abdominal-B) were required for proper genital development in O. fasciatus, and regulated Distal-less and homothorax similarly in both sexes. Appendage patterning regulation of Distal-less and dachshund was different between males and females. Knockdown of intersex produced a partial female-to-male transformation of abdominal and genital anatomy, and also resulted in abrogation of female-specific regulation of these genes. These results provide developmental genetic support for specific anatomical hypotheses of serial homology. Importantly, these gene functions and interactions describe the developmental patterning of sexually dimorphic structures that have been critical to the diversification of this species-rich insect group.