Deciphering the molecular mechanisms of mother-to-egg immune protection in the mealworm beetle Tenebrio molitor.

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.

Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort.

BACKGROUND: The disposable soma theory of ageing assumes that organisms optimally trade-off limited resources between reproduction and longevity to maximize fitness. Early reproduction should especially trade-off against late reproduction and longevity because of reduced investment into somatic protection, including immunity. Moreover, as optimal reproductive strategies of males and females differ, sexually dimorphic patterns of senescence may evolve. In particular, as males gain fitness through mating success, sexual competition should be a major factor accelerating male senescence. In a single experiment, we examined these possibilities by establishing artificial populations of the mealworm beetle, Tenebrio molitor, in which we manipulated the sex-ratio to generate variable levels of investment into reproductive effort and sexual competition in males and females. RESULTS: As predicted, variation in sex-ratio affected male and female reproductive efforts, with contrasted sex-specific trade-offs between lifetime reproduction, survival and immunity. High effort of reproduction accelerated mortality in females, without affecting immunity, but high early reproductive success was observed only in balanced sex-ratio condition. Male reproduction was costly on longevity and immunity, mainly because of their investment into copulations rather than in sexual competition. CONCLUSIONS: Our results suggest that T. molitor males, like females, maximize fitness through enhanced longevity, partly explaining their comparable longevity.

Immune priming specificity within and across generations reveals the range of pathogens affecting evolution of immunity in an insect.

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.

Trans-generational immune priming in the mealworm beetle protects eggs through pathogen-dependent mechanisms imposing no immediate fitness cost for the offspring.

Immune-challenged mothers can improve their offspring immunity through trans-generational immune priming (TGIP). In insects, TGIP endows the offspring with lifetime immunity, including the eggs, which are likely exposed soon after maternal infection. Egg protection may rely on the transfer of maternal immune effectors to the egg or/and the induction of egg immune genes. These respective mechanisms are assumed to have early-life fitness costs of different magnitude for the offspring. We provide evidence in the mealworm beetle Tenebrio molitor that enhanced egg immunity following a maternal immune challenge is achieved by both of these mechanisms but in a pathogen-dependent manner. While previously found having late-life fitness costs for the offspring, TGIP here improved egg hatching success and early larval survival, in addition of improving offspring immunity. These results suggest that early-life of primed offspring is critical in the optimization of life history trajectory of this insect under trans-generational pathogenic threats.

A dietary carotenoid reduces immunopathology and enhances longevity through an immune depressive effect in an insect model.

Immunopathology corresponds to self-damage of the inflammatory response, resulting from oxidizing molecules produced when the immune system is activated. Immunopathology often contributes to age-related diseases and is believed to accelerate ageing. Prevention of immunopathology relies on endogenous antioxidant enzymes and the consumption of dietary antioxidants, including carotenoids such as astaxanthin. Astaxanthin currently raises considerable interest as a powerful antioxidant and for its potential in alleviating age-related diseases. Current in vitro and short-term in vivo studies provide promising results about immune-stimulating and antioxidant properties of astaxanthin. However, to what extent dietary supplementation with astaxanthin can prevent long-term adverse effects of immunopathology on longevity is unknown so far. Here, using the mealworm beetle, Tenebrio molitor, as biological model we tested the effect of lifetime dietary supplementation with astaxanthin on longevity when exposed to early life inflammation. While supplementation with astaxanthin was found to lessen immunopathology cost on larval survival and insect longevity, it was also found to reduce immunity, growth rate and the survival of non immune-challenged larvae. This study therefore reveals that astaxanthin prevents immunopathology through an immune depressive effect and can have adverse consequences on growth.