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Evolution of energy metabolism in a lineage of orchid bees (Apidea : Euglossini) : from morphology to molecules Darveau, Charles-Antoine

Abstract

During hovering flight, insects reach rates of energy production that are among the highest measured in the animal kingdom, making them ideal organisms in which to study the evolution of energy metabolism. The work presented in this thesis utilised a lineage of orchid bees that covers a 20-fold range in body mass (approximately 50 - 1000 mg) to address this issue. Body mass strongly affects flight energetics and contributes to variation in metabolic rate between species, providing a useful model to investigate the correlated evolution of wholeanimal flight energetics and the design of metabolic pathways involved in energy production. At the whole-animal level, I showed that the mass-specific metabolic rate ranged from 114.4 to 37.4 ml CO₂ hr⁻¹ g⁻¹ in small and large species respectively. Similar variation in hovering flight wingbeat frequency was found for small and large species, ranging from 250 to 86 Hz, suggesting a direct relationship between these two variables. Wingbeat frequency variation was further shown to be explained by wing size and wing loading. The method of phylogenetically independent contrasts was used to demonstrate the correlated evolution of body mass independent wing loading, wingbeat frequency and mass-specific metabolic rate. The biochemical correlates associated with metabolic rate variation were also studied in orchid bee flight muscles. The activity of several enzymes of glycolysis, Krebs cycle and the electron transport chain was measured. Only for the enzyme hexokinase (HK) was there a direct relationship between its activity and the mass-specific metabolic rate during hovering flight. The activity of HK ranged from 73.8 to 19.4 U g⁻¹ thorax in small and large species respectively. The activity of HK was correlated with mass-specific metabolic rate independent of body mass or phylogenetic relatedness. The role of HK as a regulator of glycolysis and its high control of overall pathway flux appears to explain this relationship. These studies represent the first example of the biochemical alterations needed (over evolutionary time) to support changes in animal size, which is explained by the form and function associated with flight. A model addressing the scaling of metabolic rate with animal size, including the concept of multiple contributors to metabolic rate, was developed. I proposed the concept of an allometric cascade, which integrates various effects of size on the multiple contributors to metabolism involved at various levels of organisation, and tested it using data from mammals. Together, the work presented in this thesis demonstrates that the effect of body mass on animal physiology has many facets, reflecting the various aspects of animal form and function.

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