Fungal infection alters collective nutritional intake of ant colonies

Abstract

SummaryIn many animals, parasitic infections impose significant fitness costs [1–6]. Animals are known to alter their feeding behavior when infected to help combat various parasites [7–12]. For instance, they can adjust nutrient intake to support their immune system [13,14]. However, parasites can also manipulate host foraging behavior to increase their own development, survival and transmission [15–18]. The mechanisms by which nutrition influences host-parasite interactions are still not well understood. Until now, studies that examine the impact of diet on infection have mainly focused on the host, and less on the parasite [12,13, 19–25]. Using Nutritional Geometry [26], we investigated the role of key nutrients: amino acids and carbohydrates, in a host-parasite system: the Argentine ant,Linepithema humile,and the entomopathogenic fungus,Metarhizium brunneum. We first established that the fungus grew and reproduced better on diets comprising four times less amino acids than carbohydrates (1:4 AA:C ratio). Second, when facing food combinations, the fungus exploited the two complementary food resources to reach the same performance as on this optimal diet, revealing the ability of fungal pathogens to solve complex nutritional challenges. Third, when ants were fed on this optimal fungal diet, their lifespan decreased when healthy, yet not whenMetarhizium-infected, compared to their favored carbohydrate-rich diet. Interestingly, when the ants were given a binary choice between different diets, the foragers of uninfected colonies avoided intake of the fungal optimum diet, whilst choosing it when infected. Experimental disentanglement of full pathogenic infection and pure immune response to fungal cell wall material, combined with immune measurements, allowed us to conclude that this change of nutritional choice in infected ants did not result from pathogen manipulation but likely represents a compensation of the host to counterbalance the cost of using amino acids during the immune response. The observed change in foraging behavior in infected colonies towards an otherwise harmful diet (self-medication), suggests a collective compensatory mechanism for the individual cost of immunity. In short, we demonstrated that infected ants converge on a diet that is proven to be costly for survival in the long term but that could help them fight infection in the short term.HighlightsThe insect-pathogenic fungusMetarhizium brunneumperforms best on protein-rich diets and is able to solve complex nutritional challengesWhile harmful to healthy ants, protein-rich diets did not shorten infected ants’ lifespanContrary to healthy ants, when given a choice, infected and immune-stimulated ants choose a protein-rich diet