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The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils

Infectious diseases are a major threat for biodiversity conservation and can exert strong influence on wildlife population dynamics. Understanding the mechanisms driving infection rates and epidemic outcomes requires empirical data on the evolutionary trajectory of pathogens and host selective proce...

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Autores principales: Hamede, Rodrigo, Fountain‐Jones, Nicholas M., Arce, Fernando, Jones, Menna, Storfer, Andrew, Hohenlohe, Paul A., McCallum, Hamish, Roche, Benjamin, Ujvari, Beata, Thomas, Frédéric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10363845/
https://www.ncbi.nlm.nih.gov/pubmed/37492149
http://dx.doi.org/10.1111/eva.13569
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author Hamede, Rodrigo
Fountain‐Jones, Nicholas M.
Arce, Fernando
Jones, Menna
Storfer, Andrew
Hohenlohe, Paul A.
McCallum, Hamish
Roche, Benjamin
Ujvari, Beata
Thomas, Frédéric
author_facet Hamede, Rodrigo
Fountain‐Jones, Nicholas M.
Arce, Fernando
Jones, Menna
Storfer, Andrew
Hohenlohe, Paul A.
McCallum, Hamish
Roche, Benjamin
Ujvari, Beata
Thomas, Frédéric
author_sort Hamede, Rodrigo
collection PubMed
description Infectious diseases are a major threat for biodiversity conservation and can exert strong influence on wildlife population dynamics. Understanding the mechanisms driving infection rates and epidemic outcomes requires empirical data on the evolutionary trajectory of pathogens and host selective processes. Phylodynamics is a robust framework to understand the interaction of pathogen evolutionary processes with epidemiological dynamics, providing a powerful tool to evaluate disease control strategies. Tasmanian devils have been threatened by a fatal transmissible cancer, devil facial tumour disease (DFTD), for more than two decades. Here we employ a phylodynamic approach using tumour mitochondrial genomes to assess the role of tumour genetic diversity in epidemiological and population dynamics in a devil population subject to 12 years of intensive monitoring, since the beginning of the epidemic outbreak. DFTD molecular clock estimates of disease introduction mirrored observed estimates in the field, and DFTD genetic diversity was positively correlated with estimates of devil population size. However, prevalence and force of infection were the lowest when devil population size and tumour genetic diversity was the highest. This could be due to either differential virulence or transmissibility in tumour lineages or the development of host defence strategies against infection. Our results support the view that evolutionary processes and epidemiological trade‐offs can drive host‐pathogen coexistence, even when disease‐induced mortality is extremely high. We highlight the importance of integrating pathogen and population evolutionary interactions to better understand long‐term epidemic dynamics and evaluating disease control strategies.
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spelling pubmed-103638452023-07-25 The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils Hamede, Rodrigo Fountain‐Jones, Nicholas M. Arce, Fernando Jones, Menna Storfer, Andrew Hohenlohe, Paul A. McCallum, Hamish Roche, Benjamin Ujvari, Beata Thomas, Frédéric Evol Appl Original Articles Infectious diseases are a major threat for biodiversity conservation and can exert strong influence on wildlife population dynamics. Understanding the mechanisms driving infection rates and epidemic outcomes requires empirical data on the evolutionary trajectory of pathogens and host selective processes. Phylodynamics is a robust framework to understand the interaction of pathogen evolutionary processes with epidemiological dynamics, providing a powerful tool to evaluate disease control strategies. Tasmanian devils have been threatened by a fatal transmissible cancer, devil facial tumour disease (DFTD), for more than two decades. Here we employ a phylodynamic approach using tumour mitochondrial genomes to assess the role of tumour genetic diversity in epidemiological and population dynamics in a devil population subject to 12 years of intensive monitoring, since the beginning of the epidemic outbreak. DFTD molecular clock estimates of disease introduction mirrored observed estimates in the field, and DFTD genetic diversity was positively correlated with estimates of devil population size. However, prevalence and force of infection were the lowest when devil population size and tumour genetic diversity was the highest. This could be due to either differential virulence or transmissibility in tumour lineages or the development of host defence strategies against infection. Our results support the view that evolutionary processes and epidemiological trade‐offs can drive host‐pathogen coexistence, even when disease‐induced mortality is extremely high. We highlight the importance of integrating pathogen and population evolutionary interactions to better understand long‐term epidemic dynamics and evaluating disease control strategies. John Wiley and Sons Inc. 2023-06-20 /pmc/articles/PMC10363845/ /pubmed/37492149 http://dx.doi.org/10.1111/eva.13569 Text en © 2023 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Hamede, Rodrigo
Fountain‐Jones, Nicholas M.
Arce, Fernando
Jones, Menna
Storfer, Andrew
Hohenlohe, Paul A.
McCallum, Hamish
Roche, Benjamin
Ujvari, Beata
Thomas, Frédéric
The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils
title The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils
title_full The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils
title_fullStr The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils
title_full_unstemmed The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils
title_short The tumour is in the detail: Local phylogenetic, population and epidemiological dynamics of a transmissible cancer in Tasmanian devils
title_sort tumour is in the detail: local phylogenetic, population and epidemiological dynamics of a transmissible cancer in tasmanian devils
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10363845/
https://www.ncbi.nlm.nih.gov/pubmed/37492149
http://dx.doi.org/10.1111/eva.13569
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