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Facilitative priority effects drive parasite assembly under coinfection


Halliday, Fletcher W; Penczykowski, Rachel M; Barrès, Benoit; Eck, Jenalle L; Numminen, Elina; Laine, Anna-Liisa (2020). Facilitative priority effects drive parasite assembly under coinfection. Nature Ecology and Evolution, 4(11):1510-1521.

Abstract

Host individuals are often coinfected with diverse parasite assemblages, resulting in complex interactions among parasites within hosts. Within hosts, priority effects occur when the infection sequence alters the outcome of interactions among parasites. Yet, the role of host immunity in this process remains poorly understood. We hypothesized that the host response to the first infection could generate priority effects among parasites, altering the assembly of later-arriving strains during epidemics. We tested this by infecting sentinel host genotypes of Plantago lanceolata with strains of the fungal parasite Podosphaera plantaginis and measuring susceptibility to subsequent infection during experimental and natural epidemics. In these experiments, prior infection by one strain often increased susceptibility to other strains, and these facilitative priority effects altered the structure of parasite assemblages, but this effect depended on host genotype, host population and parasite genotype. Thus, host genotype, spatial structure and priority effects among strains all independently altered parasite assembly. Using a fine-scale survey and sampling of infections on wild hosts in several populations, we then identified a signal of facilitative priority effects, which altered parasite assembly during natural epidemics. Together, these results provide evidence that within-host priority effects of early-arriving strains can drive parasite assembly, with implications for how strain diversity is spatially and temporally distributed during epidemics.

Abstract

Host individuals are often coinfected with diverse parasite assemblages, resulting in complex interactions among parasites within hosts. Within hosts, priority effects occur when the infection sequence alters the outcome of interactions among parasites. Yet, the role of host immunity in this process remains poorly understood. We hypothesized that the host response to the first infection could generate priority effects among parasites, altering the assembly of later-arriving strains during epidemics. We tested this by infecting sentinel host genotypes of Plantago lanceolata with strains of the fungal parasite Podosphaera plantaginis and measuring susceptibility to subsequent infection during experimental and natural epidemics. In these experiments, prior infection by one strain often increased susceptibility to other strains, and these facilitative priority effects altered the structure of parasite assemblages, but this effect depended on host genotype, host population and parasite genotype. Thus, host genotype, spatial structure and priority effects among strains all independently altered parasite assembly. Using a fine-scale survey and sampling of infections on wild hosts in several populations, we then identified a signal of facilitative priority effects, which altered parasite assembly during natural epidemics. Together, these results provide evidence that within-host priority effects of early-arriving strains can drive parasite assembly, with implications for how strain diversity is spatially and temporally distributed during epidemics.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Scopus Subject Areas:Life Sciences > Ecology, Evolution, Behavior and Systematics
Physical Sciences > Ecology
Language:English
Date:1 November 2020
Deposited On:16 Feb 2021 13:39
Last Modified:17 Feb 2021 21:01
Publisher:Nature Publishing Group
ISSN:2397-334X
OA Status:Closed
Free access at:Related URL. An embargo period may apply.
Publisher DOI:https://doi.org/10.1038/s41559-020-01289-9
Related URLs:https://www.zora.uzh.ch/id/eprint/189448/
PubMed ID:32868915

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