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Facilitative priority effects drive parasite assembly under coinfection

Nature Ecology & Evolution volume 4, pages 1510–1521 (2020)Cite this article

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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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Fig. 1: Illustration of key differences and similarities among the three field studies presented in this manuscript.
Fig. 2: Results from the common garden experiment.
Fig. 3: Results from the natural epidemic experiment.
Fig. 4: Results from the wild host survey.

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Data availability

The data supporting the results are archived on Figshare (https://doi.org/10.6084/m9.figshare.12627806).

Code availability

The code supporting the results is archived on Figshare (https://doi.org/10.6084/m9.figshare.12627806).

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Acknowledgements

We thank P. Hyttinen, S. Neggazi, M. Kirjokangas and S. Sallinen for assistance with field and lab work. We thank J. Loehr and other staff at the Lammi Biological Station for facilitating the common garden experiment. We also thank the Nåtö Biological Station for housing in Åland. We thank K. Raveala, S. Parratt and A. Sims for additional assistance, including the processing of genetic samples. The Institute of Biotechnology and Institute for Molecular Medicine at the University of Helsinki are acknowledged for carrying out the DNA extractions and for genotyping samples, respectively. This work was supported by the University of Zürich and by grants from the Academy of Finland (no. 296686) to A.-L.L. and the European Research Council (Consolidator Grant RESISTANCE 724508) to A.-L.L.

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Author notes

  1. These authors contributed equally: Fletcher W. Halliday, Rachel M. Penczykowski.

Authors and Affiliations

  1. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland

    Fletcher W. Halliday, Jenalle L. Eck & Anna-Liisa Laine

  2. Department of Biology, Washington University in St. Louis, St. Louis, MO, USA

    Rachel M. Penczykowski

  3. Organismal & Evolutionary Biology Research Program, University of Helsinki, Helsinki, Finland

    Benoit Barrès, Elina Numminen & Anna-Liisa Laine

  4. Université de Lyon, Anses, INRAE, USC CASPER, Lyon, France

    Benoit Barrès

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Contributions

R.M.P. and A.-L.L. designed and implemented the experiments. B.B. conducted the wild host survey. J.L.E. compiled the wild host survey data. E.N. and R.M.P. resolved the parasite multilocus genotypes. F.W.H. analysed the data and wrote the first draft. All authors contributed substantially to revising the manuscript.

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Correspondence to Fletcher W. Halliday or Rachel M. Penczykowski.

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Extended data

Extended Data Fig. 1 Results from the natural epidemic experiment.

The effect of the priming treatment on a) infection severity; b) infection severity among infected hosts only. Plants were primed either 8 days (treatment P1) or 4 days (treatment P2) prior to being placed into the field. There were also C1 and C2 control plants set up at the same time (but mock inoculated). Filled points are model-estimated means, error bars are model-estimated 95% confidence intervals, and open points show the raw data. Panels are different host populations, and colors are different host genotypes. There was a significant three-way interaction in the model of infection severity. The reduced model of infection severity among infected hosts included significant two-way interactions between population and host genotype and between host genotype and experimental treatment.

Extended Data Fig. 2 Results from an unconstrained ordination of the natural epidemic experiment, showing the effect of the priming treatment on the composition of strain assemblages within hosts.

Control hosts (C1, C2) and primed hosts (P1, P2), are shown in black, and blue, respectively. Columns are different host populations, and rows are different experimental host genotypes.

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Halliday, F.W., Penczykowski, R.M., Barrès, B. et al. Facilitative priority effects drive parasite assembly under coinfection. Nat Ecol Evol 4, 1510–1521 (2020). https://doi.org/10.1038/s41559-020-01289-9

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