Disentangling the interaction among host resources, the immune system and pathogens

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.

Too much of a good thing: resource provisioning alters infectious disease dynamics in wildlife

“…However, when host susceptibility dropped sharply in response to provisioning, prevalence was minimized or pathogen eradication occurred at intermediate resource levels. This pattern runs opposite of that predicted in other theoretical models [7,12,16] and suggests an important role of immune defence in resolving observed outcomes in which supplemental resources have decreased prevalence or catalysed epidemics.…”

“…These provisioned populations also showed the highest prevalence of antibodies to West Nile virus, but authors were unable to distinguish whether higher seroprevalence was owing to increased exposure to urban vectors or recovery from disease via abundant resources [14]. Furthermore, although conceptual and mechanistic models have explored the influence of host resources on individual infection outcomes [15,16] and asked how provisioning will alter select components of R 0 (e.g. contact rate and population size [7,12]), the interactions between individual-and population-level effects and their net epidemiological outcomes have not been fully explored.…”

Resource limitation alters the consequences of co-infection for both hosts and parasites

“…Indirect interactions between parasites and host immunity also arise because immune responses often depend on resource availability (French et al, 2009). The effects of resource augmentation on the fitness of any single parasite can be positive or negative, depending on whether added resources are used by parasites for replication or by hosts for immune defense (Cressler et al, 2014). As such, the consequences of added resources for the outcome of co-infections are challenging to predict because positive and negative effects can arise depending on whether cooccurring parasites compete for the same resources, and whether the effects of immune interactions are antagonistic or facilitative.…”

Condition-dependent reproductive effort in frogs infected by a widespread pathogen

“…Pathogens can influence host fitness by reducing survival, and also by affecting reproductive success. A pathogen can influence reproductive success not only by reducing the total amount of resources available to a host, but also by altering the optimal pattern of resource allocation for an individual once it becomes infected [3].…”