Insect flight energetics and the evolution of size, form and function

Abstract

Flying insects vary greatly in body size and wing proportions, significantly impacting their flight energetics. Generally, the larger the insect, the slower its flight wingbeat frequency. However, variation in frequency is also explained by differences in wing proportions, where larger-winged insects tend to have lower frequencies. These associations affect the energy required for flight. The correlated evolution of flight form and function can be further defined using a lineage of closely related bee species varying in body mass. The decline in flight wingbeat frequency with increasing size is paralleled by flight mass-specific metabolic rate. The specific scaling exponents observed can be predicted from the wing area allometry, where a greater increase (hyperallometry) leads to a more pronounced effect on flight energetics, and hypoallometry can lead to no change in frequency and metabolic rate across species. The metabolic properties of the flight muscles also vary with body mass and wing proportions, as observed from the activity of glycolytic enzymes and the phospholipid compositions of muscle tissue, connecting morphological differences with muscle metabolic properties. The evolutionary scaling observed across species is recapitulated within species. The static allometry observed within the bumblebee Bombus impatiens, where the wing area is proportional and isometric, affects wingbeat frequency and metabolic rate, which is predicted to decrease with an increase in size. Intraspecific variation in flight muscle tissue properties is also related to flight metabolic rate. The role of developmental processes and phenotypic plasticity in explaining intraspecific differences is central to our understanding of flight energetics. These studies provide a framework where static allometry observed within species gives rise to evolutionary allometry, connecting the evolution of size, form, and function associated with insect flight.