Host characteristics and environmental factors differentially drive the burden and pathogenicity of an ectoparasite: a multilevel causal analysis.

1. Understanding the ecological factors driving the burden and pathogenicity of parasites is challenging. Indeed, the dynamics of host-parasite interactions is driven by factors organized across nested hierarchical levels (e.g. hosts, localities), and indirect effects are expected owing to interactions between levels. 2. In this study, we combined Bayesian multilevel models, path analyses and a model selection procedure to account for these complexities and to decipher the relative effects of host- and environment-related factors on the burden and the pathogenicity of an ectoparasite (Tracheliastes polycolpus) on its fish host (Leuciscus leuciscus). We also tested the year-to-year consistency of the relationships linking these factors to the burden and the pathogenic effects of T. polycolpus. 3. We found significant relationships between the parasite burden and host-related factors: body length and age were positively related to parasite burden and heterozygous hosts displayed a higher parasite burden. In contrast, both host- and environment-related factors were linked to pathogenic effects. Pathogenicity was correlated negatively with host body length and positively with age; this illustrates that some factors (e.g. body length) showed inverse relationships with parasite burden and pathogenicity. Pathogenic effects were stronger in cooler upstream sites and where host density was lower. Path analyses revealed that these relationships between environment-related factors and pathogenic effects were direct and were not indirect relationships mediated by the host characteristics. Finally, we found that the strength and the shape of certain relationships were consistent across years, while they were clearly not for some others. 4. Our study illustrates that considering conjointly causal relationships among factors and the hierarchical structure of host-parasite interactions is appropriate for dissecting the complex links between hosts, parasites and their common environment.