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.
Highlights
Over the last decade a wealth of new evidence has been put forward to demonstrate that invertebrate immune systems can possess forms of immune memory and are sometimes capable of highly specific responses (Contreras-Garduño et al, 2016; Milutinovicand Kurtz, 2016; Cooper and Eleftherianos, 2017)
transgenerational immune priming (TGIP) by Injection of Adults Is Transmitted to the F2 Generation In T. castaneum, immune priming by injection of heat-killed bacteria into adults has been shown to provide a survival benefit upon bacterial challenge to their offspring (i.e., F1 generation) when they had become adults themselves (Roth et al, 2010)
Within the beetles that received an injection challenge, there was a tendency toward TGIP, as we observed a trend toward increased survival in the paternally injection primed group compared to the priming control (N = 69, X2 = 3.401, p = 0.065; Figure 2A)
Summary
Over the last decade a wealth of new evidence has been put forward to demonstrate that invertebrate immune systems can possess forms of immune memory and are sometimes capable of highly specific responses (Contreras-Garduño et al, 2016; Milutinovicand Kurtz, 2016; Cooper and Eleftherianos, 2017). The phenomenon enabling a stronger and faster immune response upon. Immune priming can be achieved by introducing a sublethal dose of the parasite, an incapacitated, e.g., heat killed agent or using only specific molecules from the original pathogen, e.g., lipopolysaccharides (Contreras-Garduño et al, 2016; Milutinovicand Kurtz, 2016). The priming agent is most commonly introduced via septic wounding and deposition into the haemocoel or orally via feeding (Milutinovicand Kurtz, 2016). Abiotic factors, e.g., thermal exposure have been shown to prompt this phenomenon (Wojda and Taszłow, 2013; Eggert et al, 2015)
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