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Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids

BACKGROUND: Mathematical modelling of host-parasite systems has seen tremendous developments and broad applications in theoretical and applied ecology. The current study focuses on the infection dynamics of a gyrodactylid-fish system. Previous experimental studies have explored the infrapopulation d...

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Autores principales: Twumasi, Clement, Jones, Owen, Cable, Joanne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9508750/
https://www.ncbi.nlm.nih.gov/pubmed/36153606
http://dx.doi.org/10.1186/s13071-022-05471-9
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author Twumasi, Clement
Jones, Owen
Cable, Joanne
author_facet Twumasi, Clement
Jones, Owen
Cable, Joanne
author_sort Twumasi, Clement
collection PubMed
description BACKGROUND: Mathematical modelling of host-parasite systems has seen tremendous developments and broad applications in theoretical and applied ecology. The current study focuses on the infection dynamics of a gyrodactylid-fish system. Previous experimental studies have explored the infrapopulation dynamics of co-infecting ectoparasites, Gyrodactylus turnbulli and G. bullatarudis, on their fish host, Poecilia reticulata, but questions remain about parasite microhabitat preferences, host survival and parasite virulence over time. Here, we use more advanced statistics and a sophisticated mathematical model to investigate these questions based on empirical data to add to our understanding of this gyrodactylid-fish system. METHODS: A rank-based multivariate Kruskal-Wallis test coupled with its post-hoc tests and graphical summaries were used to investigate the spatial and temporal parasite distribution of different gyrodactylid strains across different host populations. By adapting a multi-state Markov model that extends the standard survival models, we improved previous estimates of survival probabilities. Finally, we quantified parasite virulence of three different strains as a function of host mortality and recovery across different fish stocks and sexes. RESULTS: We confirmed that the captive-bred G. turnbulli and wild G. bullatarudis strains preferred the caudal and rostral regions respectively across different fish stocks; however, the wild G. turnbulli strain changed microhabitat preference over time, indicating microhabitat preference of gyrodactylids is host and time dependent. The average time of host infection before recovery or death was between 6 and 14 days. For this gyrodactylid-fish system, a longer period of host infection led to a higher chance of host recovery. Parasite-related mortalities are host, sex and time dependent, whereas fish size is confirmed to be the key determinant of host recovery. CONCLUSION: From existing empirical data, we provided new insights into the gyrodactylid-fish system. This study could inform the modelling of other host-parasite interactions where the entire infection history of the host is of interest by adapting multi-state Markov models. Such models are under-utilised in parasitological studies and could be expanded to estimate relevant epidemiological traits concerning parasite virulence and host survival. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05471-9.
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spelling pubmed-95087502022-09-25 Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids Twumasi, Clement Jones, Owen Cable, Joanne Parasit Vectors Methodology BACKGROUND: Mathematical modelling of host-parasite systems has seen tremendous developments and broad applications in theoretical and applied ecology. The current study focuses on the infection dynamics of a gyrodactylid-fish system. Previous experimental studies have explored the infrapopulation dynamics of co-infecting ectoparasites, Gyrodactylus turnbulli and G. bullatarudis, on their fish host, Poecilia reticulata, but questions remain about parasite microhabitat preferences, host survival and parasite virulence over time. Here, we use more advanced statistics and a sophisticated mathematical model to investigate these questions based on empirical data to add to our understanding of this gyrodactylid-fish system. METHODS: A rank-based multivariate Kruskal-Wallis test coupled with its post-hoc tests and graphical summaries were used to investigate the spatial and temporal parasite distribution of different gyrodactylid strains across different host populations. By adapting a multi-state Markov model that extends the standard survival models, we improved previous estimates of survival probabilities. Finally, we quantified parasite virulence of three different strains as a function of host mortality and recovery across different fish stocks and sexes. RESULTS: We confirmed that the captive-bred G. turnbulli and wild G. bullatarudis strains preferred the caudal and rostral regions respectively across different fish stocks; however, the wild G. turnbulli strain changed microhabitat preference over time, indicating microhabitat preference of gyrodactylids is host and time dependent. The average time of host infection before recovery or death was between 6 and 14 days. For this gyrodactylid-fish system, a longer period of host infection led to a higher chance of host recovery. Parasite-related mortalities are host, sex and time dependent, whereas fish size is confirmed to be the key determinant of host recovery. CONCLUSION: From existing empirical data, we provided new insights into the gyrodactylid-fish system. This study could inform the modelling of other host-parasite interactions where the entire infection history of the host is of interest by adapting multi-state Markov models. Such models are under-utilised in parasitological studies and could be expanded to estimate relevant epidemiological traits concerning parasite virulence and host survival. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05471-9. BioMed Central 2022-09-24 /pmc/articles/PMC9508750/ /pubmed/36153606 http://dx.doi.org/10.1186/s13071-022-05471-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Methodology
Twumasi, Clement
Jones, Owen
Cable, Joanne
Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids
title Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids
title_full Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids
title_fullStr Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids
title_full_unstemmed Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids
title_short Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids
title_sort spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids
topic Methodology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9508750/
https://www.ncbi.nlm.nih.gov/pubmed/36153606
http://dx.doi.org/10.1186/s13071-022-05471-9
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