The impact of dietary protein and carbohydrates on gene expression in a generalist insect herbivore

ABSTRACT Nutrition fuels all of the physiological processes that animals rely on for survival and reproduction. Of all the nutrients that are required, dietary protein (p) and carbohydrates (c) have a primary role. Insect herbivores are capable of detecting amino acid and sugar concentrations in plant tissue via chemoreception and regulate their intake of these two macronutrients to reach an optimal protein:carbohydrate, or p:c, ratio, termed an intake target. A multitude of studies have shown that the two nutritional factors that have the strongest impact on insect survival and performance are dietary p:c ratio and total macronutrient content, which is the proportion of the diet made up by p and c and a proxy for energy content. Variations in these two dietary traits have strong unique and interactive effects on many insect life history traits, yet the mechanisms that mediate these effects are not well understood. While many studies have documented the effect of host plant usage on gene expression, differences in plant secondary compounds between plant species and tissue types have confounded efforts to understand nutritional contributions to transcriptional changes. This study is the first to document the transcriptional effects of dietary p:c ratio and total macronutrient content in a phytophagous insect, the polyphagous moth species Helicoverpa zea . Our results show that changes in dietary p:c ratio produced a rather limited transcriptional response, while total macronutrient content had more dramatic effects on gene expression. The invariable expression of many metabolic genes across diets also suggests that H. zea larvae employ a strategy of constitutive expression to deal with nutritional imbalances rather than diet-associated changes in expression. We also observed many similarities in the transcriptional response to diets that varied from the intake target diet in different ways (c-biased, p-biased, increased energy content). This indicates that similar mechanisms are used to deal with nutritional imbalances regardless of the direction of the imbalance, and further supports the importance of nutrient regulation. HIGHLIGHTS Variations in plant macronutrients can have strong impacts on herbivore fitness Despite a wealth of studies documenting the physiological effects of macronutrient nutrition, underlying mechanisms are still ambiguous Diet protein-to-carbohydrate ratio had an unexpectedly small impact on overall transcription, while total macronutrient content had a stronger effect The transcriptional response to dietary variations away from an optimal diet was similar across diets that varied in different ways (carbohydrate-biased, protein-biased, more concentrated) Maintaining consistent consumption and constitutive expression of digestive enzymes across diets that varied in macronutrient profiles led to compensation for the most limiting dietary macronutrient