Interactions between evolved pesticide resistance and pesticide exposure
influence immunity against pathogens
Abstract
Combined exposure to stressors, including pesticides and pathogens, is
common in natural insect populations. Pesticide resistance readily
evolves in these populations and often coopts the same stress,
detoxification, and immune pathways involved in physiological responses
against primary pathogen and pesticide exposure. As a result, resistance
evolution can alter antagonism or facilitation among chemical pesticides
and pathogens in directions that remain difficult to predict. To
investigate the interactive effects of chemical pesticide resistance,
exposure, and bacterial infection on insect phenotypes, we
experimentally evolved resistance to two different classes of pesticides
(organophosphates and pyrethroids) in the red flour beetle, Tribolium
castaneum. We exposed pesticide susceptible and resistant lines to
pesticides, the entomopathogen and biocontrol agent Bacillus
thuringiensis (Bt), or both. Pesticide resistance and Bt exposure were
individually associated with slower development, indicating sub-lethal
fitness costs of resistance and infection, respectively. After
organophosphate exposure, however, beetles developed more quickly and
were more likely to survive if also exposed to Bt. We used RNAseq to
examine the interactive effects of pesticide resistance, pesticide
exposure, and Bt exposure on gene expression. Pyrethroid-resistant
insects exhibited dampened immune responses to Bt infection relative to
susceptible ones. In a similar vein, simultaneous exposure to
organophosphates and Bt resulted in muted stress-associated
transcriptional responses compared to exposure with only one factor. Our
results suggest that direct and host-mediated indirect interactions
among pathogens and pesticides may buffer the cost of exposure to host
fitness-associated traits within generations but exacerbate trade-offs
over evolutionary time.