Abstract

Trans-generational immune priming (TGIP) describes the transfer of immune stimulation to the next generation. As stress and immunity are closely connected, we here address the question whether trans-generational effects on immunity and resistance can also be elicited by a nonpathogen stress treatment of parents. General stressors have been shown to induce immunity to pathogens within individuals. However, to our knowledge, it is as of yet unknown whether stress can also induce trans-generational effects on immunity and resistance. We exposed a parental generation (mothers, fathers, or both parents) of the red flour beetle Tribolium castaneum, a species where TGIP has been previously been demonstrated, to either a brief heat or cold shock and examined offspring survival after bacterial infection with the entomopathogen Bacillus thuringiensis. We also studied phenoloxidase activity, a key enzyme of the insect innate immune system that has previously been demonstrated to be up-regulated upon TGIP. We quantified parental fecundity and offspring developmental time to evaluate whether trans-generational priming might have costs. Offspring resistance was found to be significantly increased when both parents received a cold shock. Offspring phenoloxidase activity was also higher when mothers or both parents were cold-shocked. By contrast, parental heat shock reduced offspring phenoloxidase activity. Moreover, parental cold or heat shock delayed offspring development. In sum, we conclude that trans-generational priming for resistance could not only be elicited by pathogens or pathogen-derived components, but also by more general cues that are indicative of a stressful environment. The interaction between stress responses and the immune system might play an important role also for trans-generational effects.

Highlights

  • Parasites with their negative effects on host fitness are a strong evolutionary force (Schulenburg et al 2009)

  • Ecology and Evolution published by John Wiley & Sons Ltd

  • When both parents had been exposed to cold shock, survival of offspring was highest compared to offspring survival of na€ıve parents (GLM, chi-square test = 10.886; df = 3; contrast: p3 = 0.0009)

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Summary

Introduction

Parasites with their negative effects on host fitness are a strong evolutionary force (Schulenburg et al 2009). These defences can protect offspring, which are often exposed to the same parasites as their parents (Agrawal et al 1999) Such trans-generational defences are demonstrated in vertebrates (Harvell 1990; Mousseau and Fox 1998; Agrawal et al 1999; Grindstaff et al 2003; Rolff 2007) and invertebrates, where they are denoted as transgenerational immune priming (Little and Kraaijeveld 2004; Sadd et al 2005; Moret 2006; Sadd and Schmid-Hempel 2007, 2009; Tidbury et al 2011; Zanchi et al 2011).

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