Environmental temperature dictates the developmental pace of poikilothermic animals, but it remains unclear whether this has consequences for brain wiring and function. InDrosophilatemperature scales synaptic connectivity in the visual system, yet the underlying reasons for such scaling, the generality of this scaling across neural circuits, and the functional implications for behaviour are not understood. Here we combine anatomical, functional, and theoretical approaches to gain insights into the nature and consequences of temperature dependent synaptic scaling within the fly olfactory pathway. We show that synaptic scaling leads to heterogeneous functional effects in different olfactory sub-circuits, with striking consequences for odour-driven behaviours. A first-principle model that imposes different metabolic constraints on the neural system and organism development explains these findings, and generalises to predict brain wiring under ecologically relevant temperature cycles. Our data argue that metabolic constraints dictate the extent of synaptic scaling within neural sub-circuit and that the resulting circuit architecture and function are contingent upon the availability of synaptic partners. This complex interplay between synaptic scaling and partner availability underscores the intricate impact of temperature-dependent developmental plasticity on the behaviour of poikilothermic animals.