Hymenoptera flight muscle mitochondrial function: Increasing metabolic power increases oxidative stress

• Published in: Comparative biochemistry and physiology. Part A, Molecular & integrative physiology Molecular & integrative physiology, 2019-04, Vol.230, p.115-121
• Main Authors: Hedges, Christopher P., Wilkinson, Reuben T., Devaux, Jules B.L., Hickey, Anthony J.R.
• Format: Article
• Language: English
• Subjects: Animals; Feeding Behavior; Flight muscle; Flight, Animal; Glycerol 3-phosphate dehydrogenase; Glycerolphosphate Dehydrogenase - metabolism; Hymenoptera - classification; Hymenoptera - physiology; Mitochondria; Mitochondria, Muscle - enzymology; Mitochondria, Muscle - metabolism; Oxidative Phosphorylation; Oxidative Stress; Reactive oxygen species; Reactive Oxygen Species - metabolism; Species Specificity; Wing loading
• ISSN: 1095-6433; 1531-4332
• DOI: 10.1016/j.cbpa.2019.01.002

Insect flight is a high intensity activity, but biomechanical and metabolic requirements may vary depending on life style and feeding mode. For example, bees generally feed on pollen and nectar, whereas wasps also actively hunt and scavenge heavy prey. These variations in metabolic demands may result in different capacities of metabolic pathways in flight muscle, and utilisation some of these pathways may come at a cost of increased free radical production. To examine how metabolic requirements and oxidative stress vary between species, we explored the variation in flight mechanics and metabolism of the honeybee (Apis mellifera), bumblebee (Bombus terrestris), and German wasp (Vespula germanica). Wing structures and flight muscle properties were compared alongside measures of oxygen flux and reactive oxygen species (ROS) production from permeabilised flight muscle. The wasp wing structure is best adapted for carrying heavy loads, with the highest wing aspect ratio, lowest wing loading, and highest flight muscle ratio. Bumblebees had the lowest wing aspect ratio and flight muscle ratio, and highest wing loading. Although wasps also had the highest rates of oxygen consumption during oxidative phosphorylation, oxygen consumption did not increase in the wasp muscle following chemical uncoupling, while it did for the two bee species. While mitochondrial glycerol 3-phosphate dehydrogenase (mGPDH) mediated oxygen flux was greatest in wasps, muscle fibres released greater amounts of ROS through this pathway. Overall, the wasp has maximised lifting capacities through varying wing and flight muscle mass and by maximising OXPHOS capacities, and this accompanies elevated ROS production. •Insect flight is one of the most intense metabolic activities and biomechanical and metabolic requirements vary depending on ecology.•Pollen and nectar feeding honeybees and bumblebees, were compared to omnivorous wasps, which feed on and carry heavy prey.•Differences in flight require different metabolic capacities from flight muscle mitochondria, and highly active mitochondria elevate oxidative stress.•Wing structures and flight muscle properties indicated wasp wing structures are best adapted for carrying heavy loads.•While wasps also had the highest mitochondrial respiration rates and metabolic power, they also released the most hydrogen peroxide.