Divergent immune priming responses across flour beetle life stages and populations

Abstract

Growing evidence shows that low doses of pathogens may prime the immune response in many insects, conferring subsequent protection against infection in the same developmental stage (within-life stage priming), across life stages (ontogenic priming), or to offspring (transgenerational priming). Recent work also suggests that immune priming is a costly response. Thus, depending on host and pathogen ecology and evolutionary history, tradeoffs with other fitness components may constrain the evolution of priming. However, the relative impacts of priming at different life stages and across natural populations remain unknown. We quantified immune priming responses of 10 natural populations of the red flour beetle Tribolium castaneum, primed and infected with the natural insect pathogen Bacillus thuringiensis. We found that priming responses were highly variable both across life stages and populations, ranging from no detectable response to a 13-fold survival benefit. Comparing across stages, we found that ontogenic immune priming at the larval stage conferred maximum protection against infection. Finally, we found that various forms of priming showed sex-specific associations that may represent tradeoffs or shared mechanisms. These results indicate the importance of sex-, life stage-, and population-specific selective pressures that can cause substantial divergence in priming responses even within a species. Our work highlights the necessity of further work to understand the mechanistic basis of this variability.

Keywords: Tribolium castaneum; ontogenic immune priming; transgenerational immune priming; variability; wild populations; within‐generation immune priming.

Figure 1

Different life stages of red flour beetle Tribolium castaneum

Figure 2

Experimental design to measure the strength of immune priming responses at different stages: (a) Within‐life stage priming (individuals primed and challenged as larvae (L‐WLS) or adults [A‐WLS]), (b) ontogenic priming (individuals primed as larvae and challenged as adults), and (c) transgenerational maternal priming (females primed as larvae [L‐TG] or adults [A‐TG] were paired with uninfected virgin males and their offspring were challenged). Sample sizes of challenged individuals are provided for each treatment (priming and control) and sex

Figure 3

Variation in priming response across sexes, life stages, and populations. (a) Within‐life stage immune priming (WLS) benefit in larvae and adults, (b) ontogenic (ONT) immune priming benefit, (c) transgenerational benefits of priming adult females (A‐TG), (d) transgenerational benefits of priming females at larval stage (L‐TG). Strength of immune priming response was calculated as the hazard ratio of the proportion of deaths occurring in the unprimed group compared with the primed group under a proportional hazard model. Horizontal dashed lines in each panel indicate a hazard ratio of 1. “*”and “‐” denote significant (p ≤ .05) and nonsignificant (p > .05) impact of immune priming in each stage, sex, and population. Sample sizes for each group are given in Figure 2

Figure 4

Strength of each type of immune priming response across different life stages and sexes. Strength of priming was calculated as described in Figure 3. Sample sizes for each assay are shown in Figure 2. WLS, within‐life stage immune priming, ONT, ontogenic priming; A‐TG, transgenerational benefits of priming adult females (A‐TG); L‐TG, transgenerational benefits of priming females at larval stage

Figure 5

Associations between within‐generation and transgeneration immune priming. Strength of A‐TG response in male offspring as a function of (a) strength of WLS immune priming in female adults and (b) ONT priming in males. Strength of priming was estimated as described in Figure 3. Each population (labeled) was categorized based on the presence or absence of each type of priming response (using significant hazard ratios as explained in Figure 3), and contingency tables (shown beside each panel) were used to test the association between two types of immune priming across populations. WLS, Within‐life stage immune priming; A‐TG, transgenerational benefits of priming adult females, ONT, ontogenic immune priming