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Abstract 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 theDaphnia-Pasteuriamodel system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak ofPasteuria ramosainDaphnia 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.
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Multispecies interactions and the community context of the evolution of virulence
Pairwise host–parasite relationships are typically embedded in broader networks of ecological interactions, which have the potential to shape parasite evolutionary trajectories. Understanding this ‘community context’ of pathogen evolution is vital for wildlife, agricultural and human systems alike, as pathogens typically infect more than one host—and these hosts may have independent ecological relationships. Here, we introduce an eco-evolutionary model examining ecological feedback across a range of host–host interactions. Specifically, we analyse a model of the evolution of virulence of a parasite infecting two hosts exhibiting competitive, mutualistic or exploitative relationships. We first find that parasite specialism is necessary for inter-host interactions to impact parasite evolution. Furthermore, we find generally that increasing competition between hosts leads to higher shared parasite virulence while increasing mutualism leads to lower virulence. In exploitative host–host interactions, the particular form of parasite specialization is critical—for instance, specialization in terms of onward transmission, host tolerance or intra-host pathogen growth rate lead to distinct evolutionary outcomes under the same host–host interactions. Our work provides testable hypotheses for multi-host disease systems, predicts how changing interaction networks may impact virulence evolution and broadly demonstrates the importance of looking beyond pairwise relationships to understand evolution in realistic community contexts.
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- Award ID(s):
- 2109860
- PAR ID:
- 10584847
- Publisher / Repository:
- Royal Society
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2031
- 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.2024.0991
