The biodiversity and abundance of worldwide insect populations is suggested to be rapidly decreasing, and descriptions of a possible catastrophic extinction event has captured the attention of both scientists and the broader public. In the ensuing search for the cause of projected declines it has become clear the responsibility cannot be placed on one factor alone. Rather, the effect can only be attributed to a series of complex interactions between existing and novel stressors faced by insect populations.
There is ever increasing evidence that the outcome of such interactions cannot be predicted based on the effects of individual stressors. A primary example of this is the impact of exposure to sub-lethal concentrations of pesticides on insect susceptibility to natural pathogens and parasites. This effect has been at least partly attributed to deleterious effects of pesticides on insect immunity.
We aimed to investigate the pesticide-immune interaction in an ecological immunology (ecoimmunology) framework, which interprets heterogeneities within immune function in the context of ecological and evolutionary pressures. We examined the impact of pesticide exposure on Tenebrio molitor immune function across multiple levels of variation, including infection virulence, sex, and mating status.
We first sought to characterise a baseline immune response using the parameters phenoloxidase (PO) and pro-phenoloxidase (proPO) activity, hemocyte density and hemolymph protein concentration. We measured the response to a virulent (entomopathogenic fungus Beauveria bassiana) pathogen and a non-virulent (rat tapeworm Hymenolepis diminuta) parasite in both males and females over the infection period. We found distinct, sex-specific strategies in response to the different pathogens. Females demonstrated a more robust immune response than males, indicated by higher immune activity following B. bassiana exposure, earlier immune activation upon H. diminuta infection and a lower H. diminuta parasite load.
Following on from these findings, we next observed the immune reaction when exposed to both infection and a chemical stressor, the pesticide alpha-cypermethrin. Our findings suggested both sex of the host and virulence of the infection altered the outcome of the pesticide-infection interaction considerably. The combination of B. bassiana and alphacypermethrin exposure had a deleterious effect on mortality, and a pesticide-immune interaction was found in male beetles resulting in reduced PO activity. Consistent with previous findings, female PO activity was higher than males and unaffected by dual stressors.
In addition to immune parameters, we measured detoxification enzymes cytochrome P450, general esterases and glutathione-s-transferase following H. diminuta infection and alphacypermethrin exposure to allow comparison of immune and detoxification processes. Contrary to our predictions, there were some indications that both detoxification and immune responses were enhanced during dual exposure.
To further investigate how differences in life-history impact the response to dual-stressors we measured immune parameters and detoxification enzymes during the B. bassiana-alphacypermethrin interaction with the additional variable of host mating-status. While detoxification enzymes were again enhanced, PO activity was significantly decreased and was negatively correlated with the detoxification enzymes cytochrome P450 and general esterases. This finding is suggestive of a trade-off between immune and detoxification processes. Female T. molitor again appeared to allocate more resources towards immunity, as well as detoxification enzymes, and mated beetles of both sexes had reduced immune activity. Our results supported the hypothesis that the immune-detoxification interaction is shaped by differences in life-histories and the resource allocation hypothesis, and we discuss possible mechanisms and selective pressures contributing to this effect.
Throughout this work we found considerable evidence for an impact of pesticides on immune function, although it appeared these impacts are highly dependent on the context which they occur in. We suggest an eco-immunological framework is a useful approach to interpret the impacts of pesticides on natural insect populations.