The structure of Hymenoptera flight muscles and mitochondria at the peak of aerobic performance: a comparative electron microscope study

Abstract

It is known that the highly specialised insect indirect fibrillar flight muscles are capable of over a million consecutive wing beats achieving astonishing contraction rates of beyond a thousand successive contractions per sixty minutes of flight. Given these statistics, it is estimated that insect flight burns 2000 cal/g of muscle when experiencing sixty minutes of flight. Surprisingly, this value exceeds the maximum rate of work done by the human leg or heart muscle by 30-50 fold. Given the information, one can understand why flying insects adequately achieve the highest known rates of mass-specific aerobic metabolism. Due to these characteristics of flying insects, indirect fibrillar or asynchronous flight muscle fibres are the ideal candidates to investigate the relationship between their function, ultrastructure and aerobic metabolism. In this study we compared the asynchronous indirect muscle fibre and mitochondria ultrastructure between three closely related Hymenoptera species, the bumblebee (Bombus terrestris), honeybee (Apis mellifera) and wasp (Vespula germanica), to establish the correlation between muscle specialisation and high cellular respiration rates during aerobic metabolism. We employed transmission electron microscopy together with computational software (ImageJ) to determine myofibril diameter, sarcomere length and volume along with mitochondrial length, width and volume in all three Hymenoptera species respectively. Interestingly even though all three Hymenoptera species displayed typical asynchronous characteristics, it had been the Bombus terrestris myofibrils that had the smallest overall average. Surprisingly, Bombus terrestris also had the smallest mitochondria with regards to length, width and surface area or volume. Not surprisingly, Apis mellifera had the largest mitochondria which correlate with preceding research stating that honeybees have some of the highest mass-specific metabolism rates ever recorded. Vespula germanica mitochondria were only slightly smaller than Apis mellifera. This thesis provides an excellent foundation for the determination of an existing link between muscle specialisation in indirect fibrillar flight muscle and aerobic metabolism.