Infection by multiple pathogens of the same host is ubiquitous in both natural and managed habitats. While intraspecific variation in disease resistance is known to affect pathogen occurrence, how differences among host genotypes affect the assembly of pathogen communities remains untested. In our experiment using cloned replicates of naive Plantago lanceolata plants as sentinels during a seasonal virus epidemic, we find non-random co-occurrence patterns of five focal viruses. Using joint species distribution modelling, we attribute the non-random virus occurrence patterns primarily to differences among host genotypes and local population context. Our results show that intraspecific variation among host genotypes may play a large, previously unquantified role in pathogen community structure.

Understanding how variation in hosts, parasites, and the environment shapes patterns of disease is key to predicting ecological and evolutionary outcomes of epidemics. Yet in spatially structured populations, variation in host resistance may be spatially confounded with variation in parasite dispersal and environmental factors that affect disease processes. To tease apart these disease drivers, we paired surveys of natural epidemics with experiments manipulating spatial variation in host susceptibility to infection. We mapped epidemics of the wind‐dispersed powdery mildew pathogen Podosphaera plantaginis in five populations of its plant host, Plantago lanceolata. At 15 replicate sites within each population, we deployed groups of healthy potted ‘sentinel’ plants from five allopatric host lines. By tracking which sentinels became infected in the field and measuring pathogen connectivity and microclimate at those sites, we could test how variation in these factors affected disease when spatial variation in host resistance and soil conditions was minimized. We found that the prevalence and severity of sentinel infection varied over small spatial scales in the field populations, largely due to heterogeneity in pathogen prevalence on wild plants and unmeasured environmental factors. Microclimate was critical for disease spread only at the onset of epidemics, where humidity increased infection risk. Sentinels were more likely to become infected than initially healthy wild plants at a given field site. However, in a follow‐up laboratory inoculation study we detected no significant differences between wild and sentinel plant lines in their qualitative susceptibility to pathogen isolates from the field populations, suggesting that primarily non‐genetic differences between sentinel and wild hosts drove their differential infection rates in the field. Our study leverages a multi‐faceted experimental approach to disentangle important biotic and abiotic drivers of disease patterns within wild populations.

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Interactions among parasite species coinfecting the same host individual can have far reaching consequences for parasite ecology and evolution. How these within-host interactions affect epidemics may depend on two non-exclusive mechanisms: parasite growth and reproduction within hosts, and parasite transmission between hosts. Yet, how these two mechanisms operate under coinfection, and how sensitive they are to the composition of the coinfecting parasite community, remains poorly understood. Here, we test the hypothesis that the relationship between within- and between-host transmission of the fungal pathogen, Phomopsis subordinaria, is affected by co-occurring parasites infecting the host plant, Plantago lanceolata. We conducted a field experiment manipulating the parasite community of transmission source plants, then tracked P. subordinaria within-host transmission, as well as between-host transmission to naïve recipient plants. We find that coinfection with the powdery mildew pathogen, Podosphaera plantaginis, causes increased between-host transmission of P. subordinaria by affecting the number of infected flower stalks in the source plants, resulting from altered auto-infection. In contrast, coinfection with viruses did not have an effect on either within- or between-host transmission. We then analyzed data on the occurrence of P. subordinaria in 2018 and the powdery mildew in a multi-year survey data set from natural host populations to test whether the positive association predicted by our experimental results is evident in field epidemiological data. Consistent with our experimental findings, we observed a positive association in the occurrence of P. subordinaria and historical powdery mildew persistence. Jointly, our experimental and epidemiological results suggest that within- and between-host transmission of P. subordinaria depends on the identity of coinfecting parasites, with potentially far-reaching effects on disease dynamics and parasite co-occurrence patterns in wild populations.

The trade‐off between within‐host infection rate and transmission to new hosts is predicted to constrain pathogen evolution, and to maintain polymorphism in pathogen populations. Pathogen life‐history stages and their correlations that underpin infection development may change under coinfection with other parasites as they compete for the same limited host resources. Cross‐kingdom interactions are common among pathogens in both natural and cultivated systems, yet their impacts on disease ecology and evolution are rarely studied. The host plant Plantago lanceolata is naturally infected by both Phomopsis subordinaria, a seed killing fungus, as well as Plantago lanceolata latent virus (PlLV) in the Åland Islands, SW Finland. We performed an inoculation assay to test whether coinfection with PlLV affects performance of two P. subordinaria strains, and the correlation between within‐host infection rate and transmission potential. The strains differed in the measured life‐history traits and their correlations. Moreover, we found that under virus coinfection, within‐host infection rate of P. subordinaria was smaller but transmission potential was higher compared to strains under single infection. The negative correlation between within‐host infection rate and transmission potential detected under single infection became positive under coinfection with PlLV. To understand whether within‐host and between‐host dynamics are correlated in wild populations, we surveyed 260 natural populations of P. lanceolata for P. subordinaria infection occurrence. When infections were found, we estimated between‐hosts dynamics by determining pathogen population size as the proportion of infected individuals, and within‐host dynamics by counting the proportion of infected flower stalks in 10 infected plants. In wild populations, the proportion of infected flower stalks was positively associated with pathogen population size. Jointly, our results suggest that the trade‐off between within‐host infection load and transmission may be strain specific, and that the pathogen life‐history that underpin epidemics may change depending on the diversity of infection, generating variation in disease dynamics.