Parasite-Mediated Anorexia and Nutrition Modulate Virulence Evolution

Abstract

Temporary but substantial reductions in voluntary food intake routinely accompany parasite infection in hosts ranging from insects to humans. This "parasite-mediated anorexia" drives dynamic nutrient-dependent feedbacks within and among hosts, which should alter the fitness of both hosts and parasites. Yet, few studies have examined the evolutionary and epidemiological consequences of this ubiquitous but overlooked component of infection. Moreover, numerous biomedical, veterinary, and farming practices (e.g., rapid biomass production via high-calorie or high-fat diets, low-level antibiotics to promote growth, nutritional supplementation, nonsteroidal anti-inflammatory drugs like Ibuprofen) directly or indirectly alter the magnitude of host anorexia-while also controlling host diet and therefore the nutrients available to hosts and parasites. Here, we show that anorexia can enhance or diminish disease severity, depending on whether the current dietary context provides nutrients that bolster or inhibit immune function. Feedbacks driven by nutrition-mediated competition between host immune function and parasite production can create a unimodal relationship between anorexia and parasite fitness. Subsequently, depending on the host's diet, medical or husbandry practices that suppress anorexia could backfire, and inadvertently select for more virulent parasites and larger epidemics. These findings carry implications for the development of integrated treatment programs that consider links between host feeding behavior, nutrition, and disease severity.