Regulated apoptosis is a conserved mechanism pausing female reproduction and establishes the sterile worker caste in the eusocial wasp, Polistes

Abstract

Female reproduction is an energetically expensive process, so species evolve to balance survival with reproductive output. Many female organisms can temporarily pause their reproduction, including egg development, in response to physiological stress. The cellular mechanisms initiating and maintaining a stress-induced pause in oogenesis have been most extensively studied in Drosophila melanogaster. While the molecular control of paused oogenesis in response to starvation have been well characterized in flies, it remains unknown if these mechanisms are shared by other species with regulated pauses in oogenesis. Eusocial insects are characterized by a reproductive division of labor, with colonies of reproductive queens and sterile female workers. The social paper wasp, Polistes, has a dynamic dominance-based hierarchy for queen status. Worker Polistes are kept sterile by a combination of social and nutritional stressors. Here, we establish Polistes as a model to explore adult female reproductive plasticity. Through immunohistochemistry we have directly compared the Drosophila and Polistes ovarian structure and identified critical regions of the ovary in wasps that undergo regulated cell elimination during reproductive pause in flies. By comparing tissue structure, cell organization and rates of cell death between Polistes queens and workers we identified apoptosis as a key regulator maintaining worker sterility. Critically, this mechanism appears to be partially conserved with that in Drosophila. Finally, we find that changes in the timing and location of cell death in Polistes workers implicate oocyte identity and oocyte growth as additional potential regulators of temporary disruption of oogenesis. Summary StatementEstablishing the social paper wasp, Polistes, as a new model for female adult reproductive plasticity via temporary pausing of oogenesis in the sterile female workers.