Impact of temperature on the development and function of Drosophila melanogaster’s olfactory system

Abstract

The assembly of neural circuits during development is shaped by both intrinsic genetic programs and extrinsic environmental conditions. In insects, brain development undergoes extensive remodeling during metamorphosis, and temperature is a key environmental determinant of ectothermic development. However, how temperature-dependent changes in neuronal growth translate into circuit wiring and function remains poorly understood. Therefore, in this dissertation, I address four central questions: (1) how developmental temperature influences wiring in the Drosophila melanogaster olfactory system; (2) whether temperature-induced changes in wiring alter olfactory processing; (3) how changes in wiring due to temperature can be mechanistically linked to biophysical effects on growth; and (4) which developmental and molecular pathways mediate temperature-dependent effects on neural circuits. I show that developmental temperature systematically scales olfactory receptor neurons connectivity within the olfactory pathway, altering synaptic organization and neural growth. Odor representations remain robust, even as network connectivity is rescaled. In contrast, odor-driven behavior is stronger in flies developed at lower temperatures, which could be explained by a modified connectivity to the next downstream area. To explain these findings, I introduce a biophysical model in which temperature-dependent differences in metabolic reaction rates across cell types generate temporal mismatches during development, leading to predictable changes in neural wiring. At the molecular level, I find that temperature-induced rewiring does not arise from major changes in systemic developmental timing signals. Instead, temperature modulates the timing of downstream transcriptional programs: ecdysone-responsive transcription factors and genes involved in central energy metabolism are expressed earlier at lower temperatures. These results suggest that temperature shapes developmental outcomes by altering the temporal coordination of transcriptional and metabolic programs. Together, this work provides a multi-level view of how temperature influences neural development, linking environmental conditions to metabolism, developmental tempo, and circuit organization. It highlights how layers of the nervous systems can remain functionally robust while retaining flexibility in wiring to environmental variation, offering new insights into the effects of temperature into brain development.