Quantitative Support for the Metabolic Load Hypothesis: Metabolic Rate Measures Reveal Host-Dependent Growth Costs in...

The interactions between phytophagous insects and their host plants show a strong trend toward specialization. However, the reasons behind this trend remain largely unclear, at both the evolutionary and mechanistic level. One possible explanation is an increased energy expenditure for digesting and metabolizing more challenging hosts included in a broader host repertoire, which may reduce the energy available for other processes such as growth and development ("metabolic load hypothesis"). Differences in the performance across various hosts could reflect such costs. Using the polyphagous Polygonia c-album (comma butterfly), we tested whether observed performance differences can be linked to variation in the energetic requirements. For this, we measured the metabolic rate of larvae feeding on three different host plants and converted it into the amount of CO₂ produced per gram of mass gain ("growth cost") to assess how much energy is allocated to growth vs. digestion and assimilation. The metabolic rate of larvae feeding on a chemically more challenging plant (Ribes uva-crispa) was similar to that of individuals on the host supporting the highest growth rate (Urtica dioica). However, larvae on Ribes uva-crispa exhibited a higher energy demand per unit of growth and a lower growth rate, indicating a different energy allocation in growing larvae than when they were reared on a chemically less challenging plant. Our findings suggest that energy expenditure for digesting different hosts varies and can have direct consequences for larval performance. This indicates that the trend toward ecological specialization may, at least partly, be driven by selection to reduce the energetic costs for detoxification and digestion, in support of the metabolic load hypothesis.