The double‐edged sword of immune defence and damage control: do food availability and immune challenge alter the balance?

Abstract

Summary Animal immune systems must adaptively balance aggressive immune resistance (ability to destroy pathogens) with infection tolerance (ability to withstand the negative effects of infection; e.g. immunopathology or damage due to pathogen metabolism). Insects offer unique insight into this balancing act because phenoloxidase (PO)‐mediated melanization is a key feature of immune resistance, but PO activation obligates the production of nonspecific reactive species that can cause self‐damage. The antioxidant glutathione (GSH) can provide protection against such reactive molecules, but high levels of GSH can impair melanization. In support of the hypothesis that GSH can protect insects (e.g. crickets) from self‐damage during an immune response, we found that bacterially infected crickets showed a significant positive relationship between GSH haemolymph concentration and fecundity after controlling for bacterial growth rate. That is, GSH may be a mechanism of infection tolerance because it correlated with fecundity despite bacterial proliferation. Next, we factorially manipulated food availability and immune activation in female crickets to examine whether the relative balance between a component of immune resistance (i.e. PO) and protection from self‐damage (i.e. GSH) was plastic and sensitive to environmental conditions. Glutathione and PO were positively correlated, and the PO:GSH ratio was robust and not affected by food availability or immune activation. Thus, increased investment in a mechanism of immune resistance may obligate a concomitant increase in GSH to reduce self‐damage (i.e. increase infection tolerance). Chronic immune activation led to greater tolerance of oxidative stress suggesting that repeated immune activation upregulates infection tolerance mechanisms. Food limitation led to reduced PO activity, but not GSH concentration. This result suggests that mechanisms of immune resistance may be more sensitive to resource scarcity than mechanisms of infection tolerance. We demonstrate that some mechanisms of immune resistance and infection tolerance can be correlated and that they can be affected by food availability or immune activation.

Sexual signals reveal males’ oxidative stress defences: Testing this hypothesis in an invertebrate

“…For example, immune challenge affects wing spot size and oxidative stress impacts wing spot colour. Given that the immune response and oxidative stress are interconnected mechanisms (Costantini & Møller, ; Stahlschmidt, Acker, Kovalko, & Adamo, ), the interplay between immunity, oxidative status and SSC development should be further examined (Contreras‐Garduño & Canales‐Lazcano, ).…”

Resilience to heat waves in the aquatic snail Lymnaea stagnalis: Additive and interactive effects with micropollutants

“…Immune defence can be affected by many extrinsic factors, such as temperature (Martin, Hopkins, Mydlarz, & Rohr, ; Thomas & Blanford, ), resource level (Stahlschmidt, Acker, Kovalko, & Adamo, ) and pollutants (Martin et al., ). Heat waves may critically impair invertebrate immunocompetence (e.g.…”

“…Immune defence can be affected by many extrinsic factors, such as temperature (Martin, Hopkins, Mydlarz, & Rohr, 2010;Thomas & Blanford, 2003), resource level (Stahlschmidt, Acker, Kovalko, & Adamo, 2015) and pollutants (Martin et al, 2010 (Minchella, 1984) and/or fecundity (Lafferty & Kuris, 1999;Minchella, 1984), the observed responses to high temperature may reduce the residual reproductive value of individuals if heat waves take place, for instance, during epidemics.…”

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

“…Although GSH is not typically thought of as part of the immune response, it plays a key role in buffering animals against both pathogen toxins (Aucoin et al, 1995) and the oxidative stress that can be generated by PO activity (Clark et al, 2010). We include it here as a likely component of 'infection tolerance' (Stahlschmidt et al, 2015). Hemolymph was deproteinated immediately after collection by centrifuging at 18,845 g for 10 min at 4°C and then adding the sample to an equal amount of metaphosphoric acid (0.1 g ml −1 , Sigma-Aldrich).…”