Metabolic constraints on growth explain how developmental temperature scales synaptic connectivity relevant for behaviour.
Environmental temperature dictates the developmental pace of poikilothermic animals. In Drosophila, brain development at lower temperature is not only slower, but it also results in different wiring outcomes. A first-principle model that imposes different metabolic constraints for the growth of the neural system and the organism explains these findings, predicts brain wiring under ecologically relevant temperature cycles and explains the non-uniform scaling of neural development across temperatures. Dissecting the circuit architecture and function of first, second and third order neurons in the olfactory system, we demonstrate that the consequences of temperature are contingent upon the availability of synaptic partners in different circuits. Despite synaptic scaling, second order neurons encode robust odor representations, while temperature dependent connectivity of third order neurons leads to differences in odor-driven behavior. Therefore some circuit specific developmental programs have evolved to support functional robustness with respect to environmental temperature, while others allow phenotypic plasticity with possible adaptive advantages.