Mapping the nutritional landscape in the yellow mealworm: testing the nutrient-mediated life-history trade-offs.

Animals must acquire an ideal amount and balance of macronutrients to optimize their performance, health and fitness. The nutritional landscape provides an integrative framework for analysing how animal phenotypes are associated with multiple nutritional components. Here, we applied this powerful approach to examine how the intake of protein and carbohydrate affects nutrient acquisition and performance in the yellow mealworm (Tenebrio molitor) reared on one of 42 synthetic foods varying in protein and carbohydrate content. Tenebrio molitor larvae increased their food consumption rate in response to nutrient dilution, but this increase was not sufficient to fully compensate for the dilution. Diluting the food nutrient content with cellulose reduced the efficiency of post-ingestive nutrient utilization, further restricting macronutrient acquisition. Tenebrio molitor larvae utilized macronutrients most efficiently at a protein to carbohydrate (P:C) ratio of 1.77:1, but became less efficient at imbalanced P:C ratios. Survivorship was high at high protein intake and fell with decreasing protein intake. Pupal mass and growth rate exhibited a bell-shaped landscape, with the nutritional optima being located around protein-biased P:C ratios of 1.99:1 to 2.03:1 and 1.66:1 to 2.86:1, respectively. The nutritional optimum for development time was also identified at high P:C ratios (1.66:1  to 5.86:1). Unlike these performance traits, lipid content was maximized at carbohydrate-biased P:C ratios of 1:3.88 to 1:3.06. When given a food choice, T. molitor larvae self-composed a slightly carbohydrate-biased P:C ratio of 1:1.24, which lies between the P:C ratios that maximize performance and lipid content. Our findings indicate the occurrence of a nutrient-mediated trade-off between performance and energy storage in this insect.

Behavioural and physiological regulation of protein and carbohydrates in mealworm larvae: A geometric analysis.

Protein-carbohydrate regulation in the larvae of the mealworm beetle (Tenebrio molitor L.) was analyzed using the Geometric Framework for nutrition. In this study, the ingestive and post-ingestive responses were measured from T. molitor larvae that were subjected to choice and no-choice experiments. In the choice experiment, T. moitor larvae were simultaneously presented with one of two protein-biased foods (p35:c7 or p28:c5.6) and one of two carbohydrate-biased foods (p7:c35 or p5.6:c28). T. molitor larvae selected protein and carbohydrate in a ratio close to 1:1 over the first 15 days since the start of the experiment (days 0-15), but exhibited preference for carbohydrate-biased food over the next 15 days. The average protein:carbohydrate ratio selected over days 0-30 was 1:1.24. In the no-choice experiment, T. molitor larvae were restricted to one of seven foods with different protein and carbohydrate content (p0:c42, p7:c35, p14:c28, p21:c21, p28:c14, p35:c7, or p42:c0). On the p0:c42 food, consumption was greatly suppressed and no larvae completed their development. Across a range of these foods except p0:c42, T. molitor larvae consistently over-ate the surplus nutrient in the foods and showed a pattern of nutrient balancing similar to that previously described for other nutritional generalists. Despite having consumed substantially different amounts and ratios of macronutrients as larvae, T. molitor pupae in the no-choice food treatments had similar body nutrient composition, suggesting the presence of strong homeostatic regulation for body nutrient growth. Larval survivorship was significantly lower on two extremely imbalanced foods (p7:c35 and p42:0) than on more balanced foods. T. molitor larvae reared on p7:c35 suffered reduced biomass growth and delayed development compared with those on foods with higher protein content.

Temperature-driven plasticity in nutrient use and preference in an ectotherm.

Environmental temperature has strong effects on the rate and efficiency of resource use in ectotherms, but little is known about how changes in temperature influence their diet selection patterns. Changes in temperature may alter the balance of nutrients required by ectotherms by affecting metabolism. In response to temperature changes, ectotherms are predicted to express a preference for a specific nutrient (protein or carbohydrate) to match their altered nutrient requirement. Here, we examined the nutritional consequences of mealworm beetles (Tenebrio molitor L.) that were constrained to diets varying in protein:carbohydrate balance (P:C = 1:5, 1:1, or 5:1) or offered a choice between two nutritionally complementary diets (1:5 vs. 5:1) at four different temperatures (20, 25, 30, or 35 °C). Beetles had high mortality and reduced body mass at higher temperatures. Post-ingestive use efficiencies of both protein and carbohydrate decreased as temperature rose. Warming-driven decrease in carbohydrate use efficiencies occurred most profoundly when carbohydrates were consumed excessively. When given a choice, beetles selected protein and carbohydrate equally at 25 and 30 °C, but exhibited a significant preference for carbohydrate at 35 °C. Since carbohydrate is an immediate source of energy, this warming-driven preference for carbohydrate is explicable as an adaptive response of beetles to meet increased energy needs at high temperature. Beetles exposed to 20 °C ate substantially less food, but preferentially consumed carbohydrate over protein possibly to cope with reduced energy intake. The present findings have implications for the impact of temperature on foraging and resource use in ectotherms.

Balanced intake of protein and carbohydrate maximizes lifetime reproductive success in the mealworm beetle, Tenebrio molitor (Coleoptera: Tenebrionidae).

Recent developments in insect gerontological and nutritional research have suggested that the dietary protein:carbohydrate (P:C) balance is a critical determinant of lifespan and reproduction in many insects. However, most studies investigating this important role of dietary P:C balance have been conducted using dipteran and orthopteran species. In this study, we used the mealworm beetles, Tenebrio molitor L. (Coleoptera: Tenebrionidae), to test the effects of dietary P:C balance on lifespan and reproduction. Regardless of their reproductive status, both male and female beetles had the shortest lifespan at the protein-biased ratio of P:C 5:1. Mean lifespan was the longest at P:C 1:1 for males and at both P:C 1:1 and 1:5 for females. Mating significantly curtailed the lifespan of both males and females, indicating the survival cost of mating. Age-specific egg laying was significantly higher at P:C 1:1 than at the two imbalanced P:C ratios (1:5 or 5:1) at any given age throughout their lives, resulting in the highest lifetime reproductive success at P:C 1:1. When given a choice, beetles actively regulated their intake of protein and carbohydrate to a slightly carbohydrate-biased ratio (P:C 1:1.54-1:1.64 for males and P:C 1:1.3-1:1.36 for females). The self-selected P:C ratio was significantly higher for females than males, reflecting a higher protein requirement for egg production. Collectively, our results add to a growing body of evidence suggesting the key role played by dietary macronutrient balance in shaping lifespan and reproduction in insects.

Macronutrient Balance Modulates the Temperature-Size Rule in an Ectotherm.

Most ectotherms mature at a larger body size in colder conditions, a phenomenon known as the temperature-size rule. While a number of hypotheses have been proposed to explain this rule, little work has been done to understand it from a nutritional perspective. We have used the final-instar caterpillars of Spodoptera litura to investigate how dietary protein∶carbohydrate (P∶C) balance influences the relationship between temperature and body size. The strength and direction of the thermal reaction norm for body size were significantly altered by dietary P∶C balance. The slope of the reaction norm was nearly flat for caterpillars raised on a balanced food ([Formula: see text]) but was significantly negative for those on nutritionally imbalanced foods (1∶5 or 5∶1), especially when carbohydrates were in considerable excess. These nutrient-dependent effects of temperature on body size were caused mainly by corresponding changes in body lipid storage. When allowed to choose between imbalanced diets, caterpillars increased their preference for carbohydrates to meet high energy demands at higher temperatures. The slope of the thermal reaction norm for body size was substantially reduced by such a temperature-driven shift in nutrient preference, indicating that the impact of high temperature on body size was buffered by altered food selection. This study highlights the importance of macronutrient balance as a key factor modulating the relationship between temperature and body size in ectotherms and provides a novel approach for understanding the temperature-size rule.

Geometric analysis of nutrient balancing in the mealworm beetle, Tenebrio molitor L. (Coleoptera: Tenebrionidae).

Geometric analysis of the nutritional regulatory responses was performed on an omnivorous mealworm beetle, Tenebrio molitor L. (Coleoptera: Tenebrionidae) to test whether this beetle had the capacity to balance the intake of protein and carbohydrate. We also identified the pattern of ingestive trade-off employed when the insect was forced to balance the costs of over- and under-ingesting macronutrients. When allowed to mix their diet from two nutritionally imbalanced but complementary foods (protein-biased food: p35:c7 or p28:c5.6; carbohydrate-biased food: p7:c35 or p5.6:c28), beetles of both sexes actively regulated their intake of protein and carbohydrate to a ratio of 1:1. When confined to one of seven nutritionally imbalanced foods (p0:c42, p7:c35, p14:c28, p21:c21, p28:c14, p35:c7 or p42:c0), beetles over-ingested the excessive nutrient from these foods to such an extent that all the points of protein-carbohydrate intake aligned linearly in the nutrient space, a pattern that is characteristic of generalist feeders and omnivores. Under the restricted feeding conditions, males ate more nutrients but were less efficient at retaining their body lipids than females. Body lipid content was higher on carbohydrate-rich foods and was positively correlated with starvation resistance. Our results are consistent with the prediction based on the nutritional heterogeneity hypothesis, which links the nutritional regulatory responses of insects to their diet breadth and feeding ecology.