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Co-infections of hosts by multiple pathogen species are ubiquitous, but predicting their impact on disease remains challenging. Interactions between co-infecting pathogens within hosts can alter pathogen transmission, with the impact on transmission typically dependent on the relative arrival order of pathogens within hosts (within-host priority effects). However, it is unclear how these within-host priority effects influence multi-pathogen epidemics, particularly when the arrival order of pathogens at the host-population scale varies. Here, we combined models and experiments with zooplankton and their naturally co-occurring fungal and bacterial pathogens to examine how within-host priority effects influence multi-pathogen epidemics. Epidemiological models parametrized with within-host priority effects measured at the single-host scale predicted that advancing the start date of bacterial epidemics relative to fungal epidemics would decrease the mean bacterial prevalence in a multi-pathogen setting, while models without within-host priority effects predicted the opposite effect. We tested these predictions with experimental multi-pathogen epidemics. Empirical dynamics matched predictions from the model including within-host priority effects, providing evidence that within-host priority effects influenced epidemic dynamics. Overall, within-host priority effects may be a key element of predicting multi-pathogen epidemic dynamics in the future, particularly as shifting disease phenology alters the order of infection within hosts.
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Order of arrival and nutrient supply alter outcomes of co-infection with two fungal pathogens
A pathogen arriving on a host typically encounters a diverse community of microbes that can shape priority effects, other within-host interactions and infection outcomes. In plants, environmental nutrients can drive trade-offs between host growth and defence and can mediate interactions between co-infecting pathogens. Nutrients may thus alter the outcome of pathogen priority effects for the host, but this possibility has received little experimental investigation. To disentangle the relationship between nutrient availability and co-infection dynamics, we factorially manipulated the nutrient availability and order of arrival of two foliar fungal pathogens (Rhizoctonia solaniandColletotrichum cereale) on the grass tall fescue (Lolium arundinaceum) and tracked disease outcomes. Nutrient addition did not influence infection rates, infection severity or plant biomass.Colletotrichum cerealefacilitatedR. solani, increasing its infection rate regardless of their order of inoculation. Additionally, simultaneous andC. cereale-first inoculations decreased plant growth and—in plants that did not receive nutrient addition—increased leaf nitrogen concentrations compared to uninoculated plants. These effects were partially, but not completely, explained by the duration and severity of pathogen infections. This study highlights the importance of understanding the intricate associations between the order of pathogen arrival, host nutrient availability and host defence to better predict infection outcomes.
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- Award ID(s):
- 2308472
- PAR ID:
- 10586206
- Publisher / Repository:
- The Royal Society
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2029
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2024.0915
