Abstract
Despite the presence of conserved innate immune function, many insects have evolved a variety of mechanical, chemical, and behavioral defensive responses to pathogens. Illness-induced anorexia and dietary changes are two behavioral defensive strategies found in some solitary insects, but little is known regarding the role of such behaviors in social insects, especially in ants. In the present study we examined if such reduced foraging activity exists for a social insect, the invasive fire ant Solenopsis invicta, and its viral pathogen, Solenopsis invicta virus 1 (SINV-1). Virus-free fire ant colonies were split into two colony fragments, one of which subsequently was inoculated with SINV-1. Four food resources with different macronutrient ratios were presented to both colony fragments. SINV-1-inoculated colony fragments consistently displayed reduced foraging performance (e.g., foraging intensity and recruitment efficiency), a decline in lipid intake, and a shift in dietary preference to carbohydrate-rich foods compared with virus-free fragments. These findings provide the first evidence for virus-induced behavioral responses and dietary shifts in shaping the host-pathogen interactions in fire ants. The findings also suggest a possible mechanism for how fire ant colonies respond to viral epidemics. Potential implications of these behavioral differences for current management strategies are discussed.
Highlights
Social insects have evolved sophisticated defensive systems presumably as adaptive responses to pathogens commonly encountered because of frequent social contact
While the absence of a queen was associated with reduced foraging performance in this study, the impacts of viral infection outweighed the effects associated with queen presence and played a critical role in regulating foraging patterns of S. invicta, especially foraging intensity and recruitment efficiency
Our results provide evidence for both reduced foraging activity and a change in macronutrient preferences of virus-challenged fire ants
Summary
Social insects have evolved sophisticated defensive systems presumably as adaptive responses to pathogens commonly encountered because of frequent social contact. We tested whether reduced foraging activity or changes in macronutrient preference occur in the highly social fire ant Solenopsis invicta in response to a natural viral pathogen, Solenopsis invicta virus 1 (SINV1). This virus is a positive-sense, single-stranded RNA (ssRNA) virus that apparently only infects ant species in the genus Solenopsis[9]. The discovery of SINV-1 in invasive populations of S. invicta (e.g., Taiwan12) offers an excellent opportunity to investigate the role of pathogen-induced behaviors in colony survival of S. invicta, especially during the initial colony founding stage when queens are known to experience significant stress as a result of starvation and exposure to harsh environmental conditions. Since knowledge on interplay among feeding stimulant, foraging patterns and dietary preference plays a critical role in success of bait-based management in fire ants[16], demonstration that SINV-1 induces reduced foraging activity or changes in macronutrient intake are of critical importance because alterations of feeding rates and dietary preferences may impact the efficacies of poison baits used for fire ant control and population monitoring methods
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