Regulation of somatic stem cell development through positional and proliferative signals during Drosophila melanogaster pupal ovary development resembles the framework governing adult stem cell behavior

Follicle stem cells (FSCs) in the Drosophila melanogaster ovary are maintained through independent regulation of division and differentiation to become proliferative follicle cells (FCs) to their posterior or quiescent escort cells (ECs) to their anterior. These behaviors are guided by graded extracellular Hedgehog (Hh) and Wnt signals emanating from cells anterior to FSCs and an inverse gradient of JAK-STAT pathway activity. Here, we used lineage analyses to investigate regulation of the development of ECs, FSCs, and FCs from a common set of precursors during pupation. Previous studies found that the most anterior precursors divide slowest, with quiescence spreading from the anterior over time to include all ECs, that FSCs are specified simply by their location at eclosion, and that the first FCs derive from cells that accumulate posterior to the developing germline over the first 48 h of pupation. We found that Wnt pathway activity favored conversion of precursors to more anterior adult derivatives (ECs rather than FCs), while JAK-STAT pathway activity favored posterior outcomes. Faster division, explored by altering Cyclin E activity, favored a precursor becoming an FSC. Both JAK-STAT and Hh signaling could increase precursor division rate. All of these characteristics resemble regulation of adult FSC behavior. We suggest that the regulation of both stem cell specification and maintenance by a similar set of extracellular signals, by directly influencing cell location and cell division rate, may be general features for stem cells that are specified in parallel with tissue development and that exhibit division-independent differentiation.