Dataset Information

A host immune hormone modifies parasite species interactions and epidemics: insights from a field manipulation.

ABSTRACT: Parasite epidemics can depend on priority effects, and parasite priority effects can result from the host immune response to prior infection. Yet we lack experimental evidence that such immune-mediated priority effects influence epidemics. To address this research gap, we manipulated key host immune hormones, then measured the consequences for within-host parasite interactions, and ultimately parasite epidemics in the field. Specifically, we applied plant immune-signalling hormones to sentinel plants, embedded into a wild host population, and tracked foliar infections caused by two common fungal parasites. Within-host individuals, priority effects were altered by the immune-signalling hormone, salicylic acid (SA). Scaling up from within-host interactions, hosts treated with SA experienced a lower prevalence of a less aggressive parasite, increased burden of infection by a more aggressive parasite, and experienced fewer co-infections. Together, these results indicate that by altering within-host priority effects, host immune hormones can drive parasite epidemics. This study therefore experimentally links host immune hormones to within-host priority effects and parasite epidemics, advancing a more mechanistic understanding of how interactions among parasites alter their epidemics.

SUBMITTER: Halliday FW

PROVIDER: S-EPMC6235036 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

A host immune hormone modifies parasite species interactions and epidemics: insights from a field manipulation.

Halliday Fletcher W FW Umbanhowar James J Mitchell Charles E CE

Proceedings. Biological sciences 20181107 1890

Parasite epidemics can depend on priority effects, and parasite priority effects can result from the host immune response to prior infection. Yet we lack experimental evidence that such immune-mediated priority effects influence epidemics. To address this research gap, we manipulated key host immune hormones, then measured the consequences for within-host parasite interactions, and ultimately parasite epidemics in the field. Specifically, we applied plant immune-signalling hormones to sentinel p ...[more]

PMID: 30404885

Similar Datasets

Project description:Supplemental food provided to wildlife by human activities can be more abundant and predictable than natural resources, and subsequent changes in wildlife ecology can have profound impacts on host-parasite interactions. Identifying traits of species associated with increases or decreases in infection outcomes with resource provisioning could improve assessments of wildlife most prone to disease risks in changing environments. We conducted a phylogenetic meta-analysis of 342 host-parasite interactions across 56 wildlife species and three broad taxonomic groups of parasites to identify host-level traits that influence whether provisioning is associated with increases or decreases in infection. We predicted dietary generalists that capitalize on novel food would show greater infection in provisioned habitats owing to population growth and food-borne exposure to contaminants and parasite infectious stages. Similarly, species with fast life histories could experience stronger demographic and immunological benefits from provisioning that affect parasite transmission. We also predicted that wide-ranging and migratory behaviours could increase infection risks with provisioning if concentrated and non-seasonal foods promote dense aggregations that increase exposure to parasites. We found that provisioning increased infection with bacteria, viruses, fungi and protozoa (i.e. microparasites) most for wide-ranging, dietary generalist host species. Effect sizes for ectoparasites were also highest for host species with large home ranges but were instead lowest for dietary generalists. In contrast, the type of provisioning was a stronger correlate of infection outcomes for helminths than host species traits. Our analysis highlights host traits related to movement and feeding behaviour as important determinants of whether species experience greater infection with supplemental feeding. These results could help prioritize monitoring wildlife with particular trait profiles in anthropogenic habitats to reduce infectious disease risks in provisioned populations.

Project description:BACKGROUND: A compelling demonstration of adaptation by natural selection is the ability of parasites to manipulate host behavior. One dramatic example involves fungal species from the genus Ophiocordyceps that control their ant hosts by inducing a biting behavior. Intensive sampling across the globe of ants that died after being manipulated by Ophiocordyceps suggests that this phenomenon is highly species-specific. We advance our understanding of this system by reconstructing host manipulation by Ophiocordyceps parasites under controlled laboratory conditions and combining this with field observations of infection rates and a metabolomics survey. RESULTS: We report on a newly discovered species of Ophiocordyceps unilateralis sensu lato from North America that we use to address the species-specificity of Ophiocordyceps-induced manipulation of ant behavior. We show that the fungus can kill all ant species tested, but only manipulates the behavior of those it infects in nature. To investigate if this could be explained at the molecular level, we used ex vivo culturing assays to measure the metabolites that are secreted by the fungus to mediate fungus-ant tissue interactions. We show the fungus reacts heterogeneously to brains of different ant species by secreting a different array of metabolites. By determining which ion peaks are significantly enriched when the fungus is grown alongside brains of its naturally occurring host, we discovered candidate compounds that could be involved in behavioral manipulation by O. unilateralis s.l.. Two of these candidates are known to be involved in neurological diseases and cancer. CONCLUSIONS: The integrative work presented here shows that ant brain manipulation by O. unilateralis s.l. is species-specific seemingly because the fungus produces a specific array of compounds as a reaction to the presence of the host brain it has evolved to manipulate. These studies have resulted in the discovery of candidate compounds involved in establishing behavioral manipulation by this specialized fungus and therefore represent a major advancement towards an understanding of the molecular mechanisms underlying this phenomenon.

Dataset Information

A host immune hormone modifies parasite species interactions and epidemics: insights from a field manipulation.

Publications

A host immune hormone modifies parasite species interactions and epidemics: insights from a field manipulation.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets