Quantitative support for the metabolic load hypothesis: Metabolic rate measures reveal host-dependent growth costs in a polyphagous herbivore

The interactions between phytophagous insects and their host plants show a strong trend towards specialization. However, the reasons behind this trend remain largely unclear, at both the evolutionary and mechanistic levels. 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 towards 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.

植食性昆虫（phytophagous insects）与其寄主植物之间的互作，呈现出显著的寄主专化趋势。然而，该趋势背后的成因在进化与机制两个层面仍未完全明晰。其中一种可能解释为：当取食更广寄主谱内化学防御更强的寄主时，昆虫的消化与代谢能耗会增加，进而可用于生长发育等其他生命过程的能量随之减少，即代谢负荷假说（"metabolic load hypothesis"）。不同寄主上的昆虫表现差异可反映这类能耗成本。本研究以多食性白钩蛱蝶（Polygonia c-album，俗称逗号蛱蝶）为研究对象，验证已观测到的寄主间表现差异是否与能量需求的变异相关。为此，我们测定了取食三种不同寄主植物的幼虫的代谢速率，并将其转换为单位体重增加所产生的二氧化碳量（即生长成本（"growth cost"）），以此评估生长与消化吸收之间的能量分配情况。取食化学防御更强的寄主茶藨子（Ribes uva-crispa）的幼虫，其代谢速率与取食最利于生长的寄主异株荨麻（Urtica dioica）的幼虫相近。但取食茶藨子的幼虫，其单位生长所需的能量更高，且生长速率更低，这表明与取食化学防御较弱的寄主时相比，幼虫生长过程中的能量分配模式存在差异。本研究结果表明，取食不同寄主的消化能耗存在差异，且会直接影响幼虫的生长表现。这表明，生态特化趋势至少部分源于自然选择对解毒与消化能耗的降低作用，从而支持了代谢负荷假说。