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Parasite diversity and coinfection determine pathogen infection success and host fitness.

ABSTRACT: While the importance of changes in host biodiversity for disease risk continues to gain empirical support, the influence of natural variation in parasite diversity on epidemiological outcomes remains largely overlooked. Here, we combined field infection data from 2,191 amphibian hosts representing 158 parasite assemblages with mechanistic experiments to evaluate the influence of parasite richness on both parasite transmission and host fitness. Using a guild of larval trematode parasites (six species) and an amphibian host, our experiments contrasted the effects of parasite richness vs. composition, observed vs. randomized assemblages, and additive vs. replacement designs. Consistent with the dilution effect hypothesis extended to intrahost diversity, increases in parasite richness reduced overall infection success, including infections by the most virulent parasite. However, the effects of parasite richness on host growth and survival were context dependent; pathology increased when parasites were administered additively, even when the presence of the most pathogenic species was held constant, but decreased when added species replaced or reduced virulent species, emphasizing the importance of community composition and assembly. These results were similar or stronger when community structures were weighted by their observed frequencies in nature. The field data also revealed the highly nested structure of parasite assemblages, with virulent species generally occupying basal positions, suggesting that increases in parasite richness and antagonism in nature will decrease virulent infections. Our findings emphasize the importance of parasite biodiversity and coinfection in affecting epidemiological responses and highlight the value of integrating research on biodiversity and community ecology for understanding infectious diseases.

SUBMITTER: Johnson PT

PROVIDER: S-EPMC3384156 | biostudies-literature | 2012 Jun

REPOSITORIES: biostudies-literature

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Parasite diversity and coinfection determine pathogen infection success and host fitness.

Johnson Pieter T J PT Hoverman Jason T JT

Proceedings of the National Academy of Sciences of the United States of America 20120521 23

While the importance of changes in host biodiversity for disease risk continues to gain empirical support, the influence of natural variation in parasite diversity on epidemiological outcomes remains largely overlooked. Here, we combined field infection data from 2,191 amphibian hosts representing 158 parasite assemblages with mechanistic experiments to evaluate the influence of parasite richness on both parasite transmission and host fitness. Using a guild of larval trematode parasites (six spe ...[more]

PMID: 22615371

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Project description:Repeated extinction and recolonization events generate a landscape of host populations that vary in their time since colonization. Within this dynamic landscape, pathogens that excel at invading recently colonized host populations are not necessarily those that perform best in host populations at or near their carrying capacity, potentially giving rise to divergent selection for pathogen traits that mediate the invasion process. Rarely, however, has this contention been empirically tested. Using Daphnia magna, we explored how differences in the colonization history of a host population influence the invasion success of different genotypes of the pathogen Pasteuria ramosa. By partitioning the pathogen invasion process into a series of individual steps, we show that each pathogen optimizes invasion differently when encountering host populations that vary in their time since colonization. All pathogen genotypes were more likely to establish successfully in recently colonized host populations, but the production of transmission spores was typically maximized in either the subsequent growth or stationary phase of host colonization. Integrating across the first three pathogen invasion steps (initial establishment, proliferation, and secondary infection) revealed that overall pathogen invasion success (and its variance) was, nonetheless, highest in recently colonized host populations. However, only pathogens that were slow to kill their host were able to maximize host-facilitated dispersal. This suggests that only a subset of pathogen genotypes-the less virulent and more dispersive-are more likely to encounter newly colonized host populations at the front of a range expansion or in metapopulations with high extinction rates. Our results suggest a fundamental trade-off for a pathogen between dispersal and virulence, and evidence for higher invasion success in younger host populations, a finding with clear implications for pathogen evolution in spatiotemporally dynamic settings.

Dataset Information

Parasite diversity and coinfection determine pathogen infection success and host fitness.

Publications

Parasite diversity and coinfection determine pathogen infection success and host fitness.

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