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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 practices and medical intervention of diseases. Here, we explored effects of timing of multiple infections 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 differences 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.

SUBMITTER: Karvonen A

PROVIDER: S-EPMC6824072 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Sequential infection can decrease virulence in a fish-bacterium-fluke interaction: Implications for aquaculture disease management.

Karvonen Anssi A Fenton Andy A Sundberg Lotta-Riina LR

Evolutionary applications 20190814 10

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 consec ...[more]

PMID: 31700534

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Project description:BACKGROUND:The present study aimed to identify the national prevalence of Fasciola hepatica in Irish sheep and to conduct a risk analysis assessment based on management and treatment practices in participating flocks. Also, co-infection with rumen fluke was quantified and its association with liver fluke and management practices was assessed. METHODS:A total of 305 sheep flocks were selected ensuring even national representation of the sheep population. Participating farms were asked to complete a survey questionnaire on farm management practices and submit faecal samples during the winter of 2014-2015. Pooled faecal samples were analysed for the presence of F. hepatica and co-infection with rumen fluke. Apparent and true prevalence were calculated, additionally, the rate of co-infection with rumen fluke was also obtained. Correlation and regression analyses were used for assessing associations between management practices, liver fluke infection and co-infection with rumen fluke. RESULTS:The national true prevalence of F. hepatica was 50.4% (n?=?305). Regional prevalence varied from 41% in the east to 52% in the south. Co-infection with rumen fluke was observed in 40% of the studied population and correlated with increased F. hepatica egg counts (OR?=?2.9; P???0.001). Predominant breeds were Suffolk, Texel and Horned Mountain breeds. Beef cattle were the most frequent type of other livestock present on farms and mixed species grazing was frequently reported (73%). More than half of the flocks reported a mid-to-late lambing period (March-April). Use of mountain land for grazing was of 32%. Flukicides were most commonly used twice over the autumn-winter period. Regression analyses highlighted significant association of F. hepatica status, with the presence of other livestock on farm, frequency of flukicides used during the winter and clinical presentation of liver fluke. A significant increase in eggs per gram of faeces was observed in Charollais sheep in comparison with all other breeds. Co-infection with F. hepatica and Calicophoron daubneyi was also significantly associated with the presence of other livestock on the farm, type of flukicide used and clinical fasciolosis. CONCLUSIONS:The present study provides up-to-date information on the prevalence of F. hepatica in Irish sheep and adds insight to the epidemiology of the disease. These findings will be useful for designing new holistic control measures for F. hepatica infection.

Dataset Information

Sequential infection can decrease virulence in a fish-bacterium-fluke interaction: Implications for aquaculture disease management.

Publications

Sequential infection can decrease virulence in a fish-bacterium-fluke interaction: Implications for aquaculture disease management.

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