Different types of neurons can be distinguished by the specific targeting locations and branching patterns of their dendrites, which form the blueprint for wiring the brain. Unraveling which specific signals control different aspects of dendritic architecture, such as branching and elongation, pruning and cessation of growth, territory formation, tiling, and self-avoidance requires a quantitative comparison in control and genetically manipulated neurons. The highly conserved shapes of individually identified Drosophila neurons make them well suited for the analysis of dendritic architecture principles. However, to date it remains unclear how tightly dendritic architecture principles of identified central neurons are regulated. This study uses quantitative reconstructions of dendritic architecture of an identified Drosophila flight motoneuron (MN5) with a complex dendritic tree, comprising more than 4,000 dendritic branches and 6 mm total length. MN5 contains a fixed number of 23 dendritic subtrees, which tile into distinct, nonoverlapping volumes of the diffuse motor neuropil. Across-animal comparison and quantitative analysis suggest that tiling of the different dendritic subtrees of the same neuron is caused by competitive and repulsive interactions among subtrees, perhaps allowing different dendritic compartments to be connected to different circuit elements. We also show that dendritic architecture is similar among different wildtype and GAL4 driver fly lines. Metric and topological dendritic architecture features are sufficiently constant to allow for studies of the underlying control mechanisms by genetic manipulations. Dendritic territory and certain topological measures, such as tree compactness, are most constant, suggesting that these reflect the intrinsic molecular identity of the neuron. J. Comp. Neurol. 518:2169-2185, 2010. (c) 2010 Wiley-Liss, Inc.