Understanding how stem-cell proliferation is controlled to maintain adult tissues is of fundamental importance. Drosophila oogenesis provides an attractive system to study this issue since cell production in the ovary depends on small populations of observable germ-line and somatic stem cells. By controlling the amount of protein-rich nutrients in the diet, we established conditions under which the rate of egg production varied 60-fold. Using a cell-lineage labeling system, we found that both germ-line and somatic stem cells, as well as their progeny, adjust their proliferation rates in response to nutrition. However, the number of active stem cells does not appear to change. Proliferation rates varied fourfold; the remaining 15-fold difference in egg production resulted from different frequencies of cell death at two precise developmental points: (1) the region 2a/2b transition within the germarium, and (2) stage 8 egg chambers that are entering vitellogenesis. To initiate a genetic analysis of these changes in cell proliferation and apoptosis, we show that ovarian cells require an intact insulin pathway to fully upregulate their rate of cycling in response to a protein-rich diet and to enter vitellogenesis.