Deans, C. A. | Search bioRxiv

bioRxiv2020

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

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. HIGHLIGHTSO_LIVariations in plant macronutrients can have strong impacts on herbivore fitness C_LIO_LIDespite a wealth of studies documenting the physiological effects of macronutrient nutrition, underlying mechanisms are still ambiguous C_LIO_LIDiet protein-to-carbohydrate ratio had an unexpectedly small impact on overall transcription, while total macronutrient content had a stronger effect C_LIO_LIThe 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) C_LIO_LIMaintaining consistent consumption and constitutive expression of digestive enzymes across diets that varied in macronutrient profiles led to compensation for the most limiting dietary macronutrient C_LI

physiology↗

bioRxiv2020

Gene-by-environment interactions in agricultural pest management: population effects on diet-Bt interactions in a caterpillar

Given that plant nutrient content is both spatially and temporally dynamic (Lenhart et al., 2015; Deans et al., 2016, 2018), insect herbivores are exposed to an incredible amount of nutritional variability. This variability can constrain insects to feeding on sub-optimal resources, but it can also provide an opportunity for insects to regulate their intake of specific nutrients to obtain an optimal balance. Nutrient regulation has implications for pest control strategies in agricultural systems, as the nutritional state of pest species may impact their susceptibility to insecticides. Deans et al. (2017) showed that diet macronutrient balance has significant effects on the susceptibility of Helicoverpa zea larvae to Cry1Ac, an endotoxin expressed in transgenic Bt crops. This was demonstrated using a highly inbred laboratory strain of H. zea, limiting the applicability of these results to field populations that encompass greater genetic diversity. In this study, we assessed the impact of field-relevant macronutrient variability on the efficacy of two Bt endotoxins, Cry1Ab and Cry1Ac, using three field populations collected from different geographic regions. This was done to further understand the impact of nutritional variability on Bt susceptibility and also to determine the relevance of these effects in the field. While we saw limited differences in Cry susceptibility across populations, dietary effects were highly variable. Across populations there were distinct population-level differences in the interactions between Cry concentration and diet, the type of Cry toxin impacted by diet, and the treatment diet that produced optimal survival and performance. These results show that nutrition can have strong impacts on Bt susceptibility but also that these impacts are strongly affected by genetic background in H. zea. To accurately assess Bt susceptibility in the field, including resistance monitoring, bioassay methods should incorporate the appropriate nutritional parameters and be as localized as possible.

ecology↗