Abstract

Understanding the interactions between pathogens sharing the same host can be complicated for holometabolous animals when larval and adult stages are exposed to distinct pathogens. In medically important insect vectors, the effect of pathogen exposure at the larval stage may influence susceptibility to human pathogens at the adult stage. We addressed this hypothesis in the mosquito Aedes aegypti, a major vector of arthropod-borne viruses (arboviruses), such as the dengue virus (DENV) and the chikungunya virus (CHIKV). We experimentally assessed the consequences of sub-lethal exposure to the bacterial pathogen Bacillus thuringiensis subsp. israelensis (Bti), during larval development, on arbovirus susceptibility at the adult stage in three Ae. aegypti strains that differ in their genetic resistance to Bti. We found that larval exposure to Bti significantly increased DENV susceptibility, but not CHIKV susceptibility, in the Bti-resistant strains. However, there was no major difference in the baseline arbovirus susceptibility between the Bti-resistant strains and their Bti-susceptible parental strain. Although the generality of our results remains to be tested with additional arbovirus strains, this study supports the idea that the outcome of an infection by a pathogen depends on other pathogens sharing the same host even when they do not affect the same life stage of the host. Our findings may also have implications for Bti as a mosquito biocontrol agent, indicating that the sub-optimal Bti efficacy may have counter-productive effects by increasing vector competence, at least for some combinations of arbovirus and mosquito strains.

Highlights

  • Host–pathogen interactions are often studied as a one-to-one relationship, most hosts are simultaneously or sequentially infected with several pathogens [1]

  • We examined the consequences of a sub-lethal exposure to the bacterial pathogen Bacillus thuringiensis subsp. israelensis (Bti) during larval development on susceptibility to the dengue virus (DENV) and the chikungunya virus (CHIKV) at the adult stage

  • DENV infection was significantly higher in the Bti-exposed mosquitoes of the LR3Bti (p = 0.027) and LR4A (p = 0.0006) strains relative to the unexposed controls, whereas there was no effect of Bti exposure in the Bora-Bora strain (Figure 1)

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Summary

Introduction

Host–pathogen interactions are often studied as a one-to-one relationship, most hosts are simultaneously or sequentially infected with several pathogens [1]. Pathogens sharing the same host may interact directly through competition for resources, or indirectly via the host immune response [4,5]. Understanding interactions between pathogens infecting the same host can be complicated for holometabolous animals (i.e., with complete metamorphosis) when larval and adult stages live in separate habitats and are exposed to distinct pathogens. Larval traits can have multiple, complex fitness consequences that persist across the metamorphic boundary [6]. In mosquito vectors of human pathogens, for instance, conditions experienced at the larval stage can influence adult traits underlying vectorial capacity, such as pathogen susceptibility and lifespan [7,8,9]

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