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

Abstract

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.

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

“…With age, the probability of having been exposed to microbes increases. This may explain the higher proportion of older individuals exhibiting induced antibacterial activity in their haemolymph, as insects can produce prophylactic long lasting antibacterial responses after a single bacterial challenge [67,68]. PO activity declined at week 6 in females, which is consistent with the beginning of senescence, when reproduction started to end but survival is still relatively high ( Fig.…”

Transgenerational developmental effects of immune priming in the red flour beetle Tribolium castaneum

“…Gram type of the bacteria used for priming (Dhinaut et al 2018). Immune priming beneficial to the 73 mother can even increase offspring susceptibility to the same parasite (Vantaux et al 2014).…”

Personality, immune response and reproductive success: an appraisal of the pace‐of‐life syndrome hypothesis

“…). This method has recently proven to be useful in the mealworm beetle, T. molitor , to estimate change in immunity according previous experience of the insects with bacterial pathogens (Dhinaut, Chogne & Moret ). Bt was grown overnight in 20 mL of broth medium (LB: 10 g of tryptone, 5 g of yeast extract, 10 g of NaCl in pure water, pH 7) at 28 °C.…”

“…After being assessed for their behaviour, 11-day-old (AE2 days) beetles were infected with the Grampositive bacterium, Bt (Institut Pasteur, CIP 53.1), commonly used as biological insecticide, and which is considered as a major pathogen of T. molitor (Dubuffet et al 2015). This method has recently proven to be useful in the mealworm beetle, T. molitor, to estimate change in immunity according previous experience of the insects with bacterial pathogens (Dhinaut, Chogne & Moret 2017). Bt was grown overnight in 20 mL of broth medium (LB: 10 g of tryptone, 5 g of yeast extract, 10 g of NaCl in pure water, pH 7) at 28°C.…”