Transgenerational Developmental Effects of Immune Priming in the Red Flour Beetle Tribolium castaneum

Abstract

Immune priming, the increased chance to survive a secondary encounter with a pathogen, has been described for many invertebrate species, which lack the classical adaptive immune system of vertebrates. Priming can be specific even for closely related bacterial strains, last up to the entire lifespan of an individual, and in some species, it can also be transferred to the offspring and is then called transgenerational immune priming (TGIP). In the red flour beetle Tribolium castaneum , a pest of stored grains, TGIP has even been shown to be transferred paternally after injection of adult beetles with heat-killed Bacillus thuringiensis . Here we studied whether TGIP in T. castaneum is also transferred to the second filial generation, whether it can also occur after oral and injection priming of larvae and whether it has effects on offspring development. We found that paternal priming with B. thuringiensis does not only protect the first but also the second offspring generation. Also, fitness costs of the immune priming became apparent, when the first filial generation produced fewer offspring. Furthermore, we used two different routes of exposure to prime larvae, either by injecting them with heat-killed bacteria or orally feeding them B. thuringiensis spore culture supernatant. Neither of the parental larval priming methods led to any direct benefits regarding offspring resistance. However, the injections slowed down development of the injected individuals, while oral priming with both a pathogenic and a non-pathogenic strain of B. thuringiensis delayed offspring development. The long-lasting transgenerational nature of immune priming and its impact on offspring development indicate that potentially underlying epigenetic modifications might be stable over several generations. Therefore, this form of phenotypic plasticity might impact pest control and should be considered when using products of bacterial origin against insects.

Exposure to Inactivated Deformed Wing Virus Leads to Trans-Generational Costs but Not Immune Priming in Honeybees (Apis mellifera)

“…Our results showing costs from maternal immune challenge are generally consistent with previous TGIP studies showing developmental costs for the offspring. We know that maternal immune challenges can cause tradeoffs in the offspring, like prolonged developmental time that were observed in the beetles Tenebrio molitor and Tribolium castaneum (Zanchi et al, 2011;Schulz et al, 2019). In the moth Manduca sexta the individuals developed faster, but had reduced fecundity (Trauer and Hilker, 2013).…”

Trans-generational Immune Priming in Invertebrates: Current Knowledge and Future Prospects

“…This protection that offspring receives from mothers and fathers may be more than additive and could result in a general improvement in protection against pathogens. There is a need to increase the number of studies including paternal effect to provide a more comprehensive view of the sex-dependent TGIP process (41, 42, 47).…”

“…Considering the prominent role of epigenetics in many trans-generational adaptation processes in animals and its implication in the modulation of several within-generation immune response pathways, its involvement in TGIP must be more deeply and widely investigated (116, 144, 145). It could be a notably good candidate to explain at least a part of the paternal effect and of the sustenance of TGIP effect over multiple successive generations (47, 48).…”

Immune StimulationviaWounding Alters Chemical Profiles of AdultTribolium castaneum

“…The strong and lasting activation of PO shown in T. castaneum upon Bt infection (Behrens et al, 2014) might compete for tyrosine that is also needed for the production of quinones. The broad and unspecific responses turned on after wounding seem to be costly (Schulz et al, 2019), and some of these costs might be explained by the increased production of antimicrobial secretion compounds.…”