Transgenerational transmission of Pseudomonas entomophila causes host-pathogen co-adaptation

Insect physiology is impacted by infections, including shaping the immune response to repeated pathogen exposure. Despite transgenerational inherited effects being a reemerging field, in insects, it is unclear whether parental experiences with a pathogen can influence such responses in offspring. Using Drosophila, we studied the interaction between immunity, the microbiome, and a gut pathogen across generations. Our results showed that parental challenge established a persistent infection in the population, such that offspring were chronically exposed to the pathogen. This chronic pathogen exposure impacted many hosts physiological traits but did not confer protection to re-infection with a high dose of the pathogen. Instead, we found that the transmitted infection led to a loss of pathogen virulence in offspring. Moreover, pathogen load and virulence influenced microbiome remodeling, fecundity, and starvation resistance. The present work highlights groundbreaking concepts during transgenerational interactions: the effects on microbiota and immunity during pathogen exposure, the pathogen adaptation along with the physiological adaptation in insects, in terms of immunity, stress response, and reproduction. This project has broader implications in scope and significance because, likely in nature, offspring of social insects or insects with gregarious behaviors may be exposed to less virulent pathogens than when acquired from parents, considering that the pathogens have already undergone modifications. As seen in our study, it is possible that in other insects, less virulent pathogens are transmitted to the next generations. Consequently, such pathogen experiences might depend on the pathogen state, which impacts several aspects of offspring physiology.