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In many vertebrates and invertebrates, offspring whose mothers have been exposed to pathogens can exhibit increased levels of immune activity and/or increased survival to infection. Such phenomena, called “Trans-generational immune priming” (TGIP) are expected to provide immune protection to the offspring. As the offspring and their mother may share the same environment, and consequently similar microbial threats, we expect the immune molecules present in the progeny to be specific to the microbes that immune challenged the mother. We provide evidence in the mealworm beetle Tenebrio molitor that the antimicrobial activity found in the eggs is only active against Gram-positive bacteria, even when females were exposed to Gram-negative bacteria or fungi. Fungi were weak inducers of TGIP while we obtained similar levels of anti-Gram-positive activity using different bacteria for the maternal challenge. Furthermore, we have identified an antibacterial peptide from the defensin family, the tenecin 1, which spectrum of activity is exclusively directed toward Gram-positive bacteria as potential contributor to this antimicrobial activity. We conclude that maternal transfer of antimicrobial activity in the eggs of T. molitor might have evolved from persistent Gram-positive bacterial pathogens between insect generations., Author Summary In some insects, the immunological experience of mothers is transferred to their otherwise naïve offspring, protecting them against infection. Such a maternal effect has likely evolved from selective pressure imposed by the persistence of some microbial pathogens in the environment between insect generations. If microbes are not transmitted vertically from mother to the offspring, only those able to survive in the external environment have the highest probability to infect the offspring. Therefore, early levels of immune protection transferred by mothers to their offspring might be specific of these microbes. In this study, we found that enhanced levels of antimicrobial activity in the eggs of immune challenged females of the mealworm beetle, Tenebrio molitor, were only active against Gram-positive bacteria, whatever the microorganism used for the maternal challenge. Furthermore, immune challenged females with fungi rarely transferred antimicrobial activity to their eggs. The analysis of the proteins conferring antibacterial activity in the eggs of bacterially immune-challenged mothers revealed the presence of tenecin 1, an antibacterial peptide active against Gram-positive bacteria only. These results suggest that maternal transfer of antimicrobial activity in the eggs in T. molitor might have evolved from the persistence of Gram-positive bacterial pathogens between insect generations.

International audience; In this chapter, we describe the geographically widespread genetic fixation of traits involved in Drosophila–parasitoid immune interactions and the situations where such fixation is not observed. We then discuss how the three classes of coevolutionary dynamics that can occur at the local scale (coevolutionary escalation, coevolutionary alternation and coevolutionary polymorphism), the geographic mosaic of selection, and the phylogenetic constraints may explain such evolutionary patterns and drive diversification in the interactions. Most Drosophila parasitoid traits involved in virulence are host-species specific. Directional selection (coevolutionary escalation) on such traits can lead to their fixation or on the contrary maintain their polymorphism if these traits are associated with fitness costs. When hosts targeted by different host-specific virulence systems coexist, fluctuations in selective pressures on these systems, together with the ability of Drosophila parasitoids to select the most susceptible host for parasitization, can lead to coevolutionary alternation. Finally, we discuss the potential for parasitoid diversification in relation with the fact that most observed geographic situations, for different parasitoid clades, correspond to coevolutionary cold spots, due to fixation of virulence in parasitoid taxa.