The Role of Anorexia in Resistance and Tolerance to Infections in Drosophila

Department of Microbiology and Immunology, Stanford University, Stanford, California, USA.
PLoS Biology (Impact Factor: 9.34). 08/2009; 7(7):e1000150. DOI: 10.1371/journal.pbio.1000150
Source: PubMed


Author Summary
Two routes to decreasing susceptibility to infection are resistance (the ability to clear pathogens) and tolerance (the ability to limit damage in response to pathogens). Anorexia induced by sickness puts animals into a diet-restricted state, a state that is generally believed to extend lifespan. We asked whether anorexia induced by sickness would alter the immune response. We measured the effects of diet restriction on both resistance and tolerance to two different infections in the fruit fly, Drosophila melanogaster. In one case we found that infection induced anorexia and the resulting diet restriction increased tolerance to this infection, thereby increasing survival of flies infected with this pathogen; however, this is not a universal effect. In a second case we found another pathogen that induced anorexia but here diet restriction lead to a reduction in resistance that collapsed the immune response and caused the fly to die faster. The relationship between diet restriction and immunity is complicated and must be evaluated on a pathogen-by-pathogen basis.

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Available from: David Schneider, Jun 28, 2015
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    • "Although the response of GA cockroaches is driven by gustatory deterrence and is therefore not directly toxin - induced , the feeding response to glucose - contain - ing diets by GA cockroaches is highly comparable to the feeding response observed in animals that are infected with a toxin - producing pathogen . Infected ani - mals typically reduce consumption rate ( Exton , 1997 ; Ayres & Schneider , 2009 ; Adamo et al . , 2010 ) . "
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    ABSTRACT: Animals balance their intake of specific nutrients, but little is known about how they do so when foraging in an environment with toxic resources and whether toxic foods promote adaptations that affect life history traits. In German cockroach (Blattella germanica) populations, glucose aversion has evolved in response to glucose-containing insecticidal baits. We restricted newly eclosed glucose-averse (GA) and wild-type (WT) female cockroaches to nutritionally defined diets varying in protein-to-carbohydrate (P : C) ratio (3 : 1, 1 : 1, or 1 : 3) or gave them free choice of the 3 : 1 and 1 : 3 diets, with either glucose or fructose as the sole carbohydrate source. We mea- sured consumption of each diet over 6 days and then dissected the females to measure the length of basal oocytes in their ovaries. Our results showed significantly lower consumption by GA compared to WT cockroaches when restricted to glucose-containing diets, but also lower fructose intake by GA compared to WT cockroaches when restricted to high fructose diets or given choice of fructose-containing diets. Protein intake was regulated tightly regardless of carbohydrate intake, except by GA cockroaches restricted to glucose-containing diets. Oocyte growth was completely suppressed in GA females restricted to glucose-containing diets, but also significantly slower in GA than in WT females restricted to fructose-containing diets. Our findings suggest that GA cockroaches have adapted to reduced diet breadth through endocrine adjustments which reduce requirements for energetic fuels. Our study illustrates how an evolutionary change in the chemosensory system may affect the evolution of other traits that govern animal life histories.
    Journal of Evolutionary Biology 01/2015; · 3.23 Impact Factor
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    • "This phenomenon is phylogenetically conserved, which perhaps points to a fundamental function, and a variety of adaptive benefits has been proposed (Exton 1997). Experiments in insects suggest anorexia can enhance survival during pathogen attack (Ayres & Schneider 2009) and may function to mediate conflicts between processing food and immune activity (Adamo et al. 2010). One mechanistic factor shaping these immune-induced metabolic shifts is that some immune system molecular pathways have pleiotropic roles in other physiological processes . "
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    ABSTRACT: Evolutionary ecologists frequently argue that parasite defence is costly because resources must be reallocated from other life-history traits to fuel the immune response. However, this hypothesis is rarely explicitly tested. An alternative possibility is that immune responses impair an organism's ability to acquire the resources it needs to support metabolism. Here, we disentangle these opposing hypotheses for why the activation costs of parasite resistance arise.We studied fecundity costs associated with immune stimulation in Drosophila melanogaster. Then, by measuring correlated changes in metabolic rate, food consumption and body weight, we assessed whether responses were consistent with immunity costs originating from altered resource allocation or from impaired resource acquisition.Microbial injection resulted in a 45% fecundity decrease. It also triggered a mean decline in metabolic rate of 6% and a mean reduction in food intake of 31%; body weight was unaffected. Metabolic rate downregulation was greater in males than in females, whereas declines in food ingestion were of similar magnitude in both sexes. These physiological shifts did not depend on whether microbial challenges were alive or dead, thus they resulted from immune system activation not pathogenesis.These costs of immune activation are significant for individuals that successfully resist infection and might also occur in other situations when immune responses are upregulated without infection.Whilst we found significant activation costs of resistance, our data provide no compelling evidence for the popularly argued hypothesis that immune deployment is costly because of reallocation of energetic resources to the immune system. Instead, reduction in resource acquisition due to ‘infection-induced anorexia’ may be the principal driver of metabolic changes and fecundity costs resulting from immune response activation.
    Functional Ecology 08/2014; 28(4). DOI:10.1111/1365-2435.12236 · 4.83 Impact Factor
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    • "The models developed here can provide a novel perspective on other open questions in epidemiology. For example, decreased food consumption is a common response to infection , and many studies have suggested that anorexia might be an adaptive host response (Murray & Murray 1979; Exton 1997; Ayres & Schneider 2009). The models proposed here provide a theoretical framework for exploring the adaptive value of anorexia. "
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    ABSTRACT: The interaction between the immune system and pathogens is often characterised as a predator-prey interaction. This characterisation ignores the fact that both require host resources to reproduce. Here, we propose novel theory that considers how these resource requirements can modify the interaction between the immune system and pathogens. We derive a series of models to describe the energetic interaction between the immune system and pathogens, from fully independent resources to direct competition for the same resource. We show that increasing within-host resource supply has qualitatively distinct effects under these different scenarios. In particular, we show the conditions for which pathogen load is expected to increase, decrease or even peak at intermediate resource supply. We survey the empirical literature and find evidence for all three patterns. These patterns are not explained by previous theory, suggesting that competition for host resources can have a strong influence on the outcome of disease.
    Ecology Letters 12/2013; 17(3). DOI:10.1111/ele.12229 · 10.69 Impact Factor
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