Environmental drivers of disease depend on host community context
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Curated by eLife
Evaluation Summary:
This paper provides a framework for disentangling the direct vs. indirect effects of environment on disease, which should be of broad interest across domains of ecology, epidemiology and plant biology. The authors validate this framework with a well-designed field study of plant leaf disease across a large elevational gradient. Overall, the data analyses are appropriate, but a few aspects of interpretations could be improved.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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- Ecology (eLife)
Abstract
Predicting disease risk in an era of unprecedented biodiversity and climate change is more challenging than ever, largely because when and where hosts are at greatest risk of becoming infected depends on complex relationships between hosts, parasites, and the environment. Theory predicts that host species characterized by fast-paced life-history strategies are more susceptible to infection and contribute more to transmission than their slow-paced counterparts. Hence, disease risk should increase as host community structure becomes increasingly dominated by fast-paced hosts. Theory also suggests that environmental gradients can alter disease risk, both directly, due to abiotic constraints on parasite replication and growth, and indirectly, by changing host community structure. What is more poorly understood, however, is whether environmental gradients can also alter the effect of host community structure on disease risk. We addressed these questions using a detailed survey of host communities and infection severity along a 1100m elevational gradient in southeastern Switzerland. Consistent with prior studies, increasing elevation directly reduced infection severity, which we attribute to abiotic constraints, and indirectly reduced infection severity via changes in host richness, which we attribute to encounter reduction. Communities dominated by fast pace-of-life hosts also experienced more disease. Finally, although elevation did not directly influence host community pace-of-life, the relationship between pace-of-life and disease was sensitive to elevation: increasing elevation weakened the relationship between host community pace-of-life and infection severity. This result provides the first field evidence, to our knowledge, that an environmental gradient can alter the effect of host community structure on infection severity.
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Reviewer #2 (Public Review):
Halliday et al. sampled plant communities and foliar fungal diseases along an elevation gradient in Swiss Alps, to test the potential relationship between environment, plant communities and diseases in the context of climate change. The authors confirmed that elevation can affect diseases by both abiotic and biotic factors, and, host community pace-of-life was the main driver for diseases along elevation. The topic is important and new, the study is well-designed, and the analysis is reasonable.
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Reviewer #1 (Public Review):
Halliday et al. developed a framework to disentangle the total effect of environment on disease into a direct effect and indirect effects by environment-induced change of host community and by modifying the relationships between host community and disease.
Applying this framework, the authors studied the direct and indirect effects of elevation on plant leaf disease in the Swiss Alps. They focused on host community structures as mediator of indirect effects. Host community structures were measured by host species richness, phylogenetic diversity, and community pace of life. One important finding is that the positive effect of host community pace-of-life on disease weakened as elevation increased, suggesting an important, but less appreciated, mechanism on how elevation can indirectly influence plant disease. …
Reviewer #1 (Public Review):
Halliday et al. developed a framework to disentangle the total effect of environment on disease into a direct effect and indirect effects by environment-induced change of host community and by modifying the relationships between host community and disease.
Applying this framework, the authors studied the direct and indirect effects of elevation on plant leaf disease in the Swiss Alps. They focused on host community structures as mediator of indirect effects. Host community structures were measured by host species richness, phylogenetic diversity, and community pace of life. One important finding is that the positive effect of host community pace-of-life on disease weakened as elevation increased, suggesting an important, but less appreciated, mechanism on how elevation can indirectly influence plant disease. However, since the major findings were based on the analyses with elevation but not specific environmental variables, it does not have that strong implications about the influence of global climate change on disease as the authors stated.
The developed framework on environmental effects on disease, the well-designed filed study and the large-scale dataset would all make this paper an important contribution to the field.
Overall, the statistical analyses were reasonable. However, accurate interpretations of some results would require more clarifications on the analyses.
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Evaluation Summary:
This paper provides a framework for disentangling the direct vs. indirect effects of environment on disease, which should be of broad interest across domains of ecology, epidemiology and plant biology. The authors validate this framework with a well-designed field study of plant leaf disease across a large elevational gradient. Overall, the data analyses are appropriate, but a few aspects of interpretations could be improved.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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