Search

ABSTRACT Pathogen avoidance behaviours are often assumed to be an adaptive host defence. However, there is limited experimental data on heritable, intrapopulation phenotypic variation for avoidance, a strong prerequisite for adaptive responses to selection. We investigated trophic pathogen avoidance in 122 inbred Drosophila melanogaster lines, and in a derived outbred population. Using the FlyPAD system, we tracked the feeding choice that flies made between substrates that were either clean or contained a bacterial pathogen. We uncovered significant, but weakly heritable variation in the preference index amongst fly lines. However, instead of avoidance, most lines demonstrated a preference for substrates containing several bacterial pathogens, showing avoidance only for extremely high bacterial concentrations. Bacterial preference was not associated with susceptibility to infection and was retained in flies with disrupted immune signalling. Phenotype–genotype association analysis indicated several novel genes (CG2321, CG2006, and ptp99A) associated with increased preference for the bacterial substrate, while the amino‐acid transporter sobremesa was associated with greater aversion. Given the known fitness benefits of consuming high‐protein diets, our results suggest that bacterial attraction may instead reflect a dietary preference for protein over carbohydrate. More work quantifying intrapopulation variation in avoidance behaviours is needed to fully assess its importance in host–pathogen evolutionary ecology.

Genetic variation for resistance and disease tolerance has been described in a range of species. In Drosophila melanogaster, genetic variation in mortality following systemic Drosophila C virus (DCV) infection is driven by large-effect polymorphisms in the restriction factor pastrel (pst). However, it is unclear if pst contributes to disease tolerance. We investigated systemic DCV challenges spanning nine orders of magnitude, in males and females of 10 Drosophila Genetic Reference Panel lines carrying either a susceptible (S) or resistant (R) pst allele. We find among-line variation in fly survival, viral load and disease tolerance measured both as the ability to maintain survival (mortality tolerance) and reproduction (fecundity tolerance). We further uncover novel effects of pst on host vigour, as flies carrying the R allele exhibited higher survival and fecundity even in the absence of infection. Finally, we found significant genetic variation in the expression of the JAK-STAT ligand upd3 and the epigenetic regulator of JAK-STAT G9a. However, while G9a has been previously shown to mediate tolerance of DCV infection, we found no correlation between the expression of either upd3 or G9a on fly tolerance or resistance. Our work highlights the importance of both resistance and tolerance in viral defence.

Invertebrates lack the immune machinery underlying vertebrate-like acquired immunity. However, in many insects past infection by the same pathogen can 'prime' the immune response, resulting in improved survival upon reinfection. Here, we investigated the mechanistic basis and epidemiological consequences of innate immune priming in the fruit fly Drosophila melanogaster when infected with the gram-negative bacterial pathogen Providencia rettgeri. We find that priming in response to P. rettgeri infection is a long-lasting and sexually dimorphic response. We further explore the epidemiological consequences of immune priming and find it has the potential to curtail pathogen transmission by reducing pathogen shedding and spread. The enhanced survival of individuals previously exposed to a non-lethal bacterial inoculum coincided with a transient decrease in bacterial loads, and we provide strong evidence that the effect of priming requires the IMD-responsive antimicrobial-peptide Diptericin-B in the fat body. Further, we show that while Diptericin B is the main effector of bacterial clearance, it is not sufficient for immune priming, which requires regulation of IMD by peptidoglycan recognition proteins. This work underscores the plasticity and complexity of invertebrate responses to infection, providing novel experimental evidence for the effects of innate immune priming on population-level epidemiological outcomes.