The Drosophila central brain is composed of thousands of neurons that derive from approximately 100 neuroblasts per hemisphere. Functional circuits in the brain require precise neuronal wiring and tight control of neuronal numbers. How this accurate control of neuronal numbers is achieved during neural development is largely unclear. Specifically, the role of programmed cell death in control of cell numbers has not been studied in the central brain neuroblast lineages. Here, we focus on four postembryonic neuroblast lineages in the central brain identified on the basis that they express the homeobox gene engrailed (en). For each lineage,we determine the total number of adult-specific neurons generated as well as number and pattern of en-expressing cells. We then demonstrate that programmed cell death has a pronounced effect on the number of cells in the four lineages; approximately half of the immature adult-specific neurons in three of the four lineages are eliminated by cell death during postembryonic development. Moreover, we show that programmed cell death selectively affects en-positive versus en-negative cells in a lineage-specific manner and, thus, controls the relative number of en-expressing neurons in each lineage. Furthermore, we provide evidence that Notch signaling is involved in the regulation of en expression. Based on our findings, we conclude that lineage-specific programmed cell death plays a prominent role in the generation of neuronal number and lineage diversity in the Drosophila brain.

The Drosophila brain is a highly complex structure composed of thousands of neurons that are interconnected in numerous exquisitely organized neuropil structures such as the mushroom bodies, central complex, antennal lobes, and other specialized neuropils. While the neurons of the insect brain are known to derive in a lineage‐specific fashion from a stereotyped set of segmentally organized neuroblasts, the developmental origin and neuromeric organization of the neuropil formed by these neurons is still unclear. In this study we used genetic labeling techniques to characterize the neuropil innervation pattern of engrailed ‐expressing brain lineages of known neuromeric origin. We show that the neurons of these lineages project to and form most arborizations, in particular all of their proximal branches, in the same brain neuropil compartments in embryonic, larval and adult stages. Moreover, we show that engrailed ‐positive neurons of differing neuromeric origin respect boundaries between neuromere‐specific compartments in the brain. This is confirmed by an analysis of the arborization pattern of empty spiracles ‐expressing lineages. These findings indicate that arborizations of lineages deriving from different brain neuromeres innervate a nonoverlapping set of neuropil compartments. This supports a model for neuromere‐specific brain neuropil, in which a given lineage forms its proximal arborizations predominantly in the compartments that correspond to its neuromere of origin. J. Comp. Neurol. 517:87–104, 2009. © 2009 Wiley‐Liss, Inc.