Adaptation to oral infection inD. melanogasterthrough evolution of both resistance and disease tolerance mechanisms

Abstract

AbstractPathogens exert strong selection on hosts, that evolve and deploy different defensive strategies, namely minimizing pathogen exposure (avoidance), directly promoting pathogen elimination (resistance), and/or managing the deleterious effects of illness (disease tolerance). However, how the response to pathogens partitions across these processes has never been directly assessed in a single system, let alone in the context of known adaptive trajectories under controlled selection regimes. Here, an experimental evolution system composed ofD. melanogasterand its natural pathogenP. entomophilais used to determine the role of behavioural traits, and of resistance and disease tolerance mechanisms on host adaption. We compare a population adapted to oral infection withP. entomophila(BactOral) with its control population to find no evidence for behavioural change but measurable differences in both resistance and disease tolerance. In BactOral, we identify a relative decrease in bacterial loads correlated with an increase in gut production of specific AMPs, but no differences in bacterial intake, in differential gut cell renewal rate, or in the rate of defecation, pointing to a strengthening in resistance. Additionally, we posit that disease tolerance also contributes to the adaptive response of BactOral through a tighter control of its immune response and of the deleterious effects of exposure. This study reveals a genetically complex and mechanistically multi-layered response, possibly reflecting the structure of adaptation to infection in natural populations.