Dataset Information

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.

SUBMITTER: Hite JL

PROVIDER: S-EPMC6863757 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Parasite-Mediated Anorexia and Nutrition Modulate Virulence Evolution.

Hite Jessica L JL Cressler Clayton E CE

Integrative and comparative biology 20191101 5

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 pr ...[more]

PMID: 31187120

Similar Datasets

Project description:Virulence, the degree to which a pathogen harms its host, is an important but poorly understood aspect of host-pathogen interactions. Virulence is not static, instead depending on ecological context and potentially evolving rapidly. For instance, at the start of an epidemic, when susceptible hosts are plentiful, pathogens may evolve increased virulence if this maximizes their intrinsic growth rate. However, if host density declines during an epidemic, theory predicts evolution of reduced virulence. Although well-studied theoretically, there is still little empirical evidence for virulence evolution in epidemics, especially in natural settings with native host and pathogen species. Here, we used a combination of field observations and lab assays in the Daphnia-Pasteuria model system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak of Pasteuria ramosa in Daphnia dentifera, where infection prevalence peaked at ~ 40% of the population infected and host density declined precipitously during the outbreak. In controlled infections in the lab, lifespan and reproduction of infected hosts was lower than that of unexposed control hosts and of hosts that were exposed but not infected. We did not detect any significant changes in host resistance or parasite infectivity, nor did we find evidence for shifts in parasite virulence (quantified by host lifespan and number of clutches produced by hosts). However, over the epidemic, the parasite evolved to produce significantly fewer spores in infected hosts. While this finding was unexpected, it might reflect previously quantified tradeoffs: parasites in high mortality (e.g., high predation) environments shift from vegetative growth to spore production sooner in infections, reducing spore yield. Future studies that track evolution of parasite spore yield in more populations, and that link those changes with genetic changes and with predation rates, will yield better insight into the drivers of parasite evolution in the wild.Supplementary informationThe online version contains supplementary material available at 10.1007/s10682-022-10169-6.

Project description:There is a clear need to understand the effect of human intervention on the evolution of infectious disease. In particular, culling and harvesting of both wildlife and managed livestock populations are carried out in a wide range of management practices, and they have the potential to impact the evolution of a broad range of disease characteristics. Applying eco-evolutionary theory we show that once culling/harvesting becomes targeted on specific disease classes, the established result that culling selects for higher virulence is only found when sufficient infected individuals are culled. If susceptible or recovered individuals are targeted, selection for lower virulence can occur. An important implication of this result is that when culling to eradicate an infectious disease from a population, while it is optimal to target infected individuals, the consequent evolution can increase the basic reproductive ratio of the infection, R0, and make parasite eradication more difficult. We show that increases in evolved virulence due to the culling of infected individuals can lead to excess population decline when sustainably harvesting a population. In contrast, culling susceptible or recovered individuals can select for decreased virulence and a reduction in population decline through culling. The implications to the evolution of virulence are typically the same in wildlife populations, that are regulated by the parasite, and livestock populations, that have a constant population size where restocking balances the losses due to mortality. However, the well-known result that vertical transmission selects for lower virulence and transmission in wildlife populations is less marked in livestock populations for parasites that convey long-term immunity since restocking can enhance the density of the immune class. Our work emphasizes the importance of understanding the evolutionary consequences of intervention strategies and the different ecological feedbacks that can occur in wildlife and livestock populations.

Dataset Information

Parasite-Mediated Anorexia and Nutrition Modulate Virulence Evolution.

Publications

Parasite-Mediated Anorexia and Nutrition Modulate Virulence Evolution.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets