Dietary Protein and Carbohydrates Affect Immune Function and Performance in a Specialist Herbivore Insect (Manduca sexta)

Abstract

Nutrition structures ecology and evolution across all scales of biological organization. It is well known that nutrition can have direct effects on performance and fitness, but indirect effects on physiological systems that mediate biotic interactions have been studied less frequently. Here, we focus on the interaction between nutrition, performance, and the immune system in a specialist herbivorous insect, Manduca sexta. We used a conceptual framework in nutritional ecology (the geometric framework) to examine how changes in diet quality affect aspects of the immune system used for defense against parasitoids. We raised caterpillars throughout their entire larval development on five different experimental diets that varied in protein and carbohydrate content and measured five aspects of the immune system: encapsulation, phenoloxidase activity, prophenoloxidase activity, total hemolymph protein, and hemocyte density. Overall, different parts of the immune function varied in response to interactions between carbohydrates, protein, and intake, but protein reductions had the largest impactsmostly detrimental. In addition, our data suggest that diet quality mediates the relationship between performance (growth and survival) and immune function, as well as trade-offs among different components of immune function. Our work is the first to examine the interplay between nutrition, performance, and immune function with the geometric framework in a specialist insect herbivore.

The nutritional landscape of host plants for a specialist insect herbivore

“…In Figure , we plot the nutrient rails of both young and old leaves for all species, which illustrates a few key points about the system. First, we show in previous work that M. sexta caterpillars from a long‐standing colony in our laboratory need p:c ratios of approximately 1:1 for optimal growth (Wilson et al, ). When combined with results from the current study in Figure , a few key points emerge.…”

“…Gray lines are raw values whereas black lines represent the median value for each group. The black dot represents the average target intake (1.587 g of carbohydrates and 1.894 g of protein) of a M. sexta larvae over their development (as measured by previously—Wilson et al, ). Rails to the left of the 1:1 P:C rail indicate that the larvae are protein constrained on that host‐plant species and rails to the right of the 1:1 P:C rail are carbohydrate constrained…”

“…Though growth and body size are often good proxies for fitness (Arnold, ), other physiological attributes can have consequences for survival and reproduction. Previous work has shown a strong link between different aspects of the insect immune system and nutrition (Cotter et al, ; Wilson et al, ). Our recent work on M. sexta showed interacting effects of protein and carbohydrates in experimental diets on both growth and five measures of immune function related to defense against parasitoids (encapsulation, phenoloxidase activity, prophenoloxidase activity, hemolymph protein, and hemocyte density) (Wilson et al, ).…”

“…Larvae develop through five instars and eventually descend to the ground where they bury themselves, construct a pupal chamber, and either emerge as adults in approximately 3 weeks or enter diapause and emerge the following season. The costs and benefits of the use of different host plants have been examined in terms of performance (Diamond & Kingsolver, ), fitness (Diamond & Kingsolver, ), and predator avoidance (Mira & Bernays, ), but to our knowledge, the nutritional landscape of the range of host plants available has yet to be explored, despite strong evidence for interactions between nutritional components and performance, fecundity, and immune function (Diamond & Kingsolver, , ; Wilson et al, ).…”

“…and fitness (Chen, 2008;Cotter, Simpson, Raubenheimer, & Wilson, 2010;Simpson & Raubenheimer, 2001;Wilson, Ruiz, & Davidowitz, 2019) and that these effects can cascade upward to higher trophic levels (Sznajder & Harvey, 2003), in many systems we still lack a basic understanding of the nutritional landscape offered to insect herbivores over different spatial and temporal scales.…”