In a number of species, individuals exposed to pathogens can mount an immune response and transmit this immunological experience to their offspring, thereby protecting them against persistent threats. Such vertical transfer of immunity, named trans-generational immune priming (TGIP), has been described in both vertebrates and invertebrates. Although increasingly studied during the last decade, the mechanisms underlying TGIP in invertebrates are still elusive, especially those protecting the earliest offspring life stage, i.e. the embryo developing in the egg. In the present study, we combined different proteomic and transcriptomic approaches to determine whether mothers transfer a “signal” (such as fragments of infecting bacteria), mRNA and/or protein/peptide effectors to protect their eggs against two natural bacterial pathogens, namely the Gram-positive Bacillus thuringiensis and the Gram-negative Serratia entomophila. By taking the mealworm beetle Tenebrio molitor as a biological model, our results suggest that eggs are mainly protected by an active direct transfer of a restricted number of immune proteins and of antimicrobial peptides. In contrast, the present data do not support the involvement of mRNA transfer while the transmission of a “signal”, if it happens, is marginal and only occurs within 24h after maternal exposure to bacteria. This work exemplifies how combining global approaches helps to disentangle the different scenarios of a complex trait, providing a comprehensive characterization of TGIP mechanisms in T. molitor. It also paves the way for future alike studies focusing on TGIP in a wide range of invertebrates and vertebrates to identify additional candidates that could be specific to TGIP and to investigate whether the TGIP mechanisms found herein are specific or common to all insect species.

Author summary

All living organisms are regularly exposed to a wide and diverse range of pathogens. To protect themselves, many species have developed an immune system able to detect and eradicate these pathogens. Most interestingly, this immunological experience can be transferred by parents to their offspring to protect them from pathogens that may persist in the environment and to which they could be exposed during their life. While extensively studied in vertebrates, this phenomenon–called trans-generational immune priming (TGIP)–has only been identified a decade ago in invertebrates and the supporting molecular mechanisms are still largely unknown. Recently, we proposed four different scenarios as a practical framework to investigate the mechanisms supporting this complex phenomenon. In the present study, we combined different molecular approaches to disentangle these different scenarios and provide a comprehensive characterization of maternal TGIP mechanisms in a model insect, the mealworm beetle Tenebrio molitor.