Host plant quality, selection history and trade-offs shape the immune responses ofManduca sexta

Abstract

Immune defences are an important component of fitness. Yet susceptibility to pathogens is common, suggesting the presence of ecological and evolutionary limitations on immune defences. Here, we use structural equation modelling to quantify the direct effects of resource quality and selection history, and their indirect effects mediated via body condition prior to an immune challenge on encapsulation and melanization immune defences in the tobacco hornworm, Manduca sexta. We also investigate allocation trade-offs among immune defences and growth rate following an immune challenge. We found considerable variation in the magnitude and direction of the direct effects of resource quality and selection history on immune defences and their indirect effects mediated via body condition and allocation trade-offs. Greater resource quality and evolutionary exposure to pathogens had positive direct effects on encapsulation and melanization. The indirect effect of resource quality on encapsulation mediated via body condition was substantial, whereas indirect effects on melanization were negligible. Individuals in better condition prior to the immune challenge had greater encapsulation; however, following the immune challenge, greater encapsulation traded off with slower growth rate. Our study demonstrates the importance of experimentally and analytically disentangling the relative contributions of direct and indirect effects to understand variation in immune defences.

Reconfiguration of the immune system network during food limitation in the caterpillarManduca sexta

“…Hemocyte numbers declined in low-nutrition caterpillars, but were maintained in absent-nutrition caterpillars. The decline in hemocyte number in low-nutrition caterpillars may be immunologically significant; M. sexta showed reduced encapsulation when fed a low-nutrition diet (Diamond and Kingsolver, 2011). However, changes in hemocyte number are difficult to interpret.…”

The effect of food limitation on immunity factors and disease resistance in the western tent caterpillar

“…In studies with natural plant material, Diamond and Kingsolver (2010) compared the eVect of high and low quality food plants on the immune response of Manduca sexta and found that the better quality host plant improved body condition and the encapsulation response of larvae following an immune challenge. Heliothis virescens larvae fed on cotton grew more slowly, an indication of poor food quality, and were more resistant to Autographa californica MNPV (AcMNPV) than larvae fed lettuce or artiWcial diet that supported better larval growth (Hoover et al 1998).…”

Variation in immune defence in relation to age in the green-veined white butterfly (Pieris napi L.)

“…One prerequisite for a trade-off to occur is that the involved traits are, in some way, costly to maintain or use (Siva-Jothy et al, 1998;Zuk and Stoehr, 2002). Regarding the immune defence system, there are now many studies demonstrating that there are costs involved in maintaining an immune system and that the immune functions depend on the available energy budget (e.g., Moret and Schmid-Hempel, 2000;Freitak et al, 2003;Rolff and Siva-Jothy, 2003;Schmid-Hempel, 2003;Sadd and Siva-Jothy, 2006;Diamond and Kingslover, 2011). Thus, the immune defence system is a resource based trait, important for successful reproduction and high fitness, dependent on nitrogenous reserves and nutritional status (Lee et al, 2008).…”