Trans-generational immune priming (TGIP) refers to the transfer of the parental immunological experience to its progeny. This may result in offspring protection from repeated encounters with pathogens that persist across generations. Although extensively studied in vertebrates for over a century, this phenomenon has only been identified 20 years ago in invertebrates. Since then, invertebrate TGIP has been the focus of an increasing interest, with half of studies published during the last few years. TGIP has now been tested in several invertebrate systems using various experimental approaches and measures to study it at both functional and evolutionary levels. However, drawing an overall picture of TGIP from available studies still appears to be a difficult task. Here, we provide a comprehensive review of TGIP in invertebrates with the objective of confronting all the data generated to date to highlight the main features and mechanisms identified in the context of its ecology and evolution. To this purpose, we describe all the articles reporting experimental investigation of TGIP in invertebrates and propose a critical analysis of the experimental procedures performed to study this phenomenon. We then investigate the outcome of TGIP in the offspring and its ecological and evolutionary relevance before reviewing the potential molecular mechanisms identified to date. In the light of this review, we build hypothetical scenarios of the mechanisms through which TGIP might be achieved and propose guidelines for future investigations.

Many organisms can improve their immune response as a function of their immunological experience or that of their parents. This phenomenon, called immune priming, has likely evolved from repetitive challenges by the same pathogens during the host lifetime or across generation. All pathogens may not expose host to the same probability of re-infection, and immune priming is expected to evolve from pathogens exposing the host to the greatest probability of re-infection. Under this hypothesis, the priming response to these pathogens should be specifically more efficient and less costly than to others. We examined the specificity of immune priming within and across generations in the mealworm beetle, Tenebrio molitor, by comparing survival of individuals to infection with bacteria according to their own immunological experience or that of their mother with these bacteria. We found that insects primed with Gram-positive bacteria became highly protected against both Gram-positive and Gram-negative bacterial infections, mainly due to an induced persistent antibacterial response, which did not exist in insects primed with Gram-negative bacteria. Insects primed with Gram-positive bacteria also exhibited enhanced concentration of haemocytes, but their implication in acquired resistance was not conclusive because of the persistent antibacterial activity in the haemolymph. Offspring maternally primed with Gram-positive and Gram-negative bacteria exhibited similarly improved immunity, whatever the bacteria used for the infection. Such maternal protection was costly in the larval development of offspring, but this cost was lower for offspring maternally primed with Gram-positive bacteria. While T. molitor can develop some levels of primed response to Gram-negative bacteria, the priming response to Gram-positive bacteria was more efficient and less costly. We concluded that Gram-positive bacterial pathogens were of paramount importance in the evolution of immune priming in this insect species.