Sequential infection can decrease virulence in a fish‐bacterium‐fluke interaction : implications for aquaculture disease management
Abstract
Hosts are typically infected with multiple strains or genotypes of one or several parasite species. These infections can take place simultaneously, but also at different times, i.e. sequentially, when one of the parasites establishes first. Sequential parasite dynamics are common in nature, but also in intensive farming units such as aquaculture. However, knowledge of effects of previous exposures on virulence of current infections in intensive farming is very limited. This is critical as consecutive epidemics and infection history of a host could underlie failures in management practises and medical intervention of diseases. Here, we explored effects of timing of multiple infection on virulence in two common aquaculture parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum. We exposed fish hosts first to flukes and then to bacteria in two separate experiments, altering timing between the infections from few hours to several weeks. We found that both short‐term and long‐term difference in timing of the two infections resulted in significant, genotype‐specific decrease in bacterial virulence. Second, we developed a mathematical model, parameterized from our experimental results, to predict the implications of sequential infections for epidemiological progression of the disease, and levels of fish population suppression, in an aquaculture setting. Predictions of the model showed that sequential exposure of hosts can decrease the population‐level impact of the bacterial epidemic, primarily through the increased recovery rate of sequentially infected hosts, thereby substantially protecting the population from the detrimental impact of infection. However, these effects depended on bacterial strain–fluke genotype combinations, suggesting the genetic composition of the parasite populations can greatly influence the degree of host suppression. Overall, these results suggest that host infection history can have significant consequences for the impact of infection at host population level, potentially shaping parasite epidemiology, disease dynamics and evolution of virulence in farming environments.
Main Authors
Format
Articles
Research article
Published
2019
Series
Subjects
Publication in research information system
Publisher
Wiley-Blackwell Publishing, Inc.
The permanent address of the publication
https://urn.fi/URN:NBN:fi:jyu-201911054719Use this for linking
Review status
Peer reviewed
ISSN
1752-4571
DOI
https://doi.org/10.1111/eva.12850
Language
English
Published in
Evolutionary Applications
Citation
- Karvonen, A., Fenton, A., & Sundberg, L.-R. (2019). Sequential infection can decrease virulence in a fish‐bacterium‐fluke interaction : implications for aquaculture disease management. Evolutionary Applications, 12(10), 1900-1911. https://doi.org/10.1111/eva.12850
Funder(s)
Research Council of Finland
Research Council of Finland
Research Council of Finland
Funding program(s)
Akatemiahanke, SA
Akatemiatutkija, SA
Akatemiahanke, SA
Academy Project, AoF
Academy Research Fellow, AoF
Academy Project, AoF

Additional information about funding
This work was supported by the Finnish Centre of Excellence Program of the Academy of Finland; the CoE in Biological Interactions 2012-2017 (#252411), and by the Academy of Finland grants #263864, #266879, #292763,#310632, and #314939.
Copyright© 2019 The Authors