Modular presynaptic assemblages scale to postsynaptic partner number

Behavioral diversification can arise through evolutionary and inter-individual differences in neural circuit development. In the mushroom body, which is an associative learning center of arthropods, the number of Kenyon cells (KCs) varies across species and among individuals. How such variation is developmentally accommodated by projection neurons (PNs), which provide sensory input to KCs, is not understood. In Drosophila melanogaster, we have previously demonstrated that PNs scale their presynaptic bouton number to KC population size. Here, we identify developmental mechanisms underlying this input flexibility. Boutons form on axonal collaterals; for PNs, we find that collateral number is subtype specific and serves as a substrate through which bouton number scales to KC population size. Independent of PN identity or KC number, most individual collaterals produce only one to three boutons, suggesting collaterals are modular cell biological bouton units. Developing PNs initially overproduce nascent collaterals in the early pupa. The set of nascent collaterals that form boutons and mature is conditional on KC number, thereby executing scaling. Finally, early boutons bear filopodia that contact neighboring PN processes, suggesting that bouton-bouton interactions contribute to shaping these structures.