Architecture of the insect tracheal system driven by spatially varying limitation of oxygen and carbon dioxide transport

Insects transport respiratory gases through a system of air-filled tubes (tracheae) that branch extensively to reach individual cells. A century of research has focused primarily on how tracheal systems deliver oxygen, often overlooking the complementary challenge of removing carbon dioxide. Here, we develop and analyse a model of simultaneous O₂ and CO₂ transport, which we parametrize with morphological and metabolic data. The model reveals a fundamental asymmetry: oxygen transport is most limited by the tissue gap between tracheoles and mitochondria; carbon dioxide transport, by contrast, is limited primarily by the geometry and ventilation of the air-filled parts of the system. Applying the model to Manduca sexta caterpillars shows that CO₂ accumulation is especially sensitive to tracheal diffusive capacity, narrowing of terminal tracheal tubes and ventilatory depth. These results imply a spatial partitioning of tracheal functions in which the CO₂ problem drives the capacities of air-filled parts of the system and patterns of ventilation, whereas the O₂ problem drives the arrangement and physiology of tracheoles and tracheolar-mitochondrial distances.