The Hox code abolishes anatomical variation in an insect gonad

Phenotypic traits can vary based on genes or environment. Nevertheless, some quantitative traits remain invariant. Understanding the developmental mechanisms that generate such invariance can reveal how phenotypic robustness evolves. Insect reproductive capacity is largely determined by the number of gamete-producing subunits within the gonad, providing a tractable system to investigate these mechanisms as they operate on a quantitative trait that impacts fitness. In most insects, gonad subunit number varies within and between species. Here, we investigate gonad development in the milkweed bug Oncopeltus fasciatus, wherein subunit number is invariant. We show that subunit number is established during embryogenesis, when some abdominal segments, but not others, specify somatic gonad precursors. The position and number of these precursors depend on segment identity, and experimentally modified segment number or Hox-mediated segment identity changes the number of gonad subunits. Thus, O. fasciatus establishes invariant subunit number by coupling gonad development to segmental patterning machinery. We propose that co-option of the Hox code provides a developmental mechanism for generating robustness in gonad subunit number and may thereby contribute to the evolution of reproductive capacity in other insects.