CO2 narcosis induces a metabolic shift mediated via juvenile hormone in Bombus impatiens gynes

Abstract

Carbon dioxide (CO2) has pleiotropic effects on insect physiology and behavior. Although diverse, many impacts are related to changes in metabolism and reallocation of macronutrients. Here we examined the metabolic shift induced by CO2 and its regulation using Bombus impatiens. CO2 applied to bumble bee gynes induces bypass of diapause and transition into reproduction. We analyzed ovary activation and macronutrient amounts in four tissues/body parts (fat body, thorax, ovaries, and crop) at three timepoints following CO2 administration. To tease apart the effects of CO2 on reproduction and metabolism, we monitored the metabolic changes in gynes following ovary removal and CO2 narcosis. We also explored the role of juvenile hormone in mediating CO2 impact by feeding queens with a JH antagonist (Precocene). Gynes ovary activation was increased following CO2 treatment. Additionally, CO2-treated gynes showed lower lipid amount in the fat body and higher glycogen and protein amount in the ovary ten days after the treatment. CO2 treatment following ovary removal also resulted in decreased fat body lipids, suggesting that CO2 operates by inducing a metabolic shift independent of reproduction. Lastly, gynes fed with precocence did not show a metabolic shift following CO2, suggesting CO2 impact is mediated via juvenile hormone. Overall, these data suggest that CO2 induces transfer of macronutrients and utilization of stored reserved by accelerating metabolism. The proposed mechanism of CO2 may explain many of the pleiotropic effects of CO2 across species and can aid in understanding how this common anastatic influences insect physiology.