The ecology and evolution of wildlife cancers: Applications for management and conservation

Abstract Ecological and evolutionary concepts have been widely adopted to understand host–pathogen dynamics, and more recently, integrated into wildlife disease management. Cancer is a ubiquitous disease that affects most metazoan species; however, the role of oncogenic phenomena in eco‐evolutionary...

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Main Authors: Rodrigo Hamede, Rachel Owen, Hannah Siddle, Sarah Peck, Menna Jones, Antoine M. Dujon, Mathieu Giraudeau, Benjamin Roche, Beata Ujvari, Frédéric Thomas
Format: Article
Language:English
Published: Wiley 2020-08-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.12948
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author Rodrigo Hamede
Rachel Owen
Hannah Siddle
Sarah Peck
Menna Jones
Antoine M. Dujon
Mathieu Giraudeau
Benjamin Roche
Beata Ujvari
Frédéric Thomas
spellingShingle Rodrigo Hamede
Rachel Owen
Hannah Siddle
Sarah Peck
Menna Jones
Antoine M. Dujon
Mathieu Giraudeau
Benjamin Roche
Beata Ujvari
Frédéric Thomas
The ecology and evolution of wildlife cancers: Applications for management and conservation
Evolutionary Applications
cancer
disease ecology
host–pathogen interactions
natural selection
transmissible tumour
wildlife management
author_facet Rodrigo Hamede
Rachel Owen
Hannah Siddle
Sarah Peck
Menna Jones
Antoine M. Dujon
Mathieu Giraudeau
Benjamin Roche
Beata Ujvari
Frédéric Thomas
author_sort Rodrigo Hamede
title The ecology and evolution of wildlife cancers: Applications for management and conservation
title_short The ecology and evolution of wildlife cancers: Applications for management and conservation
title_full The ecology and evolution of wildlife cancers: Applications for management and conservation
title_fullStr The ecology and evolution of wildlife cancers: Applications for management and conservation
title_full_unstemmed The ecology and evolution of wildlife cancers: Applications for management and conservation
title_sort ecology and evolution of wildlife cancers: applications for management and conservation
publisher Wiley
series Evolutionary Applications
issn 1752-4571
publishDate 2020-08-01
description Abstract Ecological and evolutionary concepts have been widely adopted to understand host–pathogen dynamics, and more recently, integrated into wildlife disease management. Cancer is a ubiquitous disease that affects most metazoan species; however, the role of oncogenic phenomena in eco‐evolutionary processes and its implications for wildlife management and conservation remains undeveloped. Despite the pervasive nature of cancer across taxa, our ability to detect its occurrence, progression and prevalence in wildlife populations is constrained due to logistic and diagnostic limitations, which suggests that most cancers in the wild are unreported and understudied. Nevertheless, an increasing number of virus‐associated and directly transmissible cancers in terrestrial and aquatic environments have been detected. Furthermore, anthropogenic activities and sudden environmental changes are increasingly associated with cancer incidence in wildlife. This highlights the need to upscale surveillance efforts, collection of critical data and developing novel approaches for studying the emergence and evolution of cancers in the wild. Here, we discuss the relevance of malignant cells as important agents of selection and offer a holistic framework to understand the interplay of ecological, epidemiological and evolutionary dynamics of cancer in wildlife. We use a directly transmissible cancer (devil facial tumour disease) as a model system to reveal the potential evolutionary dynamics and broader ecological effects of cancer epidemics in wildlife. We provide further examples of tumour–host interactions and trade‐offs that may lead to changes in life histories, and epidemiological and population dynamics. Within this framework, we explore immunological strategies at the individual level as well as transgenerational adaptations at the population level. Then, we highlight the need to integrate multiple disciplines to undertake comparative cancer research at the human–domestic–wildlife interface and their environments. Finally, we suggest strategies for screening cancer incidence in wildlife and discuss how to integrate ecological and evolutionary concepts in the management of current and future cancer epizootics.
topic cancer
disease ecology
host–pathogen interactions
natural selection
transmissible tumour
wildlife management
url https://doi.org/10.1111/eva.12948
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spelling doaj-8b00b8abe8cc4c38afe12f9a77fc018d2020-11-25T03:24:35ZengWileyEvolutionary Applications1752-45712020-08-011371719173210.1111/eva.12948The ecology and evolution of wildlife cancers: Applications for management and conservationRodrigo Hamede0Rachel Owen1Hannah Siddle2Sarah Peck3Menna Jones4Antoine M. Dujon5Mathieu Giraudeau6Benjamin Roche7Beata Ujvari8Frédéric Thomas9School of Natural Sciences University of Tasmania Hobart Tas. AustraliaCentre for Biological Sciences University of Southampton Southampton UKCentre for Biological Sciences University of Southampton Southampton UKWildlife Veterinarian, Veterinary Register of Tasmania South Hobart Tas. AustraliaSchool of Natural Sciences University of Tasmania Hobart Tas. AustraliaCentre for Integrative Ecology School of Life and Environmental Sciences Deakin University Vic. AustraliaCentre de Recherches Ecologiques et Evolutives sur le Cancer/Centre de Recherches en Ecologie et Evolution de la Santé Unité Mixte de Recherches Institut de Recherches pour le Développement 224‐Centre National de la Recherche Scientifique 5290‐Université de Montpellier Montpellier FranceCentre de Recherches Ecologiques et Evolutives sur le Cancer/Centre de Recherches en Ecologie et Evolution de la Santé Unité Mixte de Recherches Institut de Recherches pour le Développement 224‐Centre National de la Recherche Scientifique 5290‐Université de Montpellier Montpellier FranceSchool of Natural Sciences University of Tasmania Hobart Tas. AustraliaCentre de Recherches Ecologiques et Evolutives sur le Cancer/Centre de Recherches en Ecologie et Evolution de la Santé Unité Mixte de Recherches Institut de Recherches pour le Développement 224‐Centre National de la Recherche Scientifique 5290‐Université de Montpellier Montpellier FranceAbstract Ecological and evolutionary concepts have been widely adopted to understand host–pathogen dynamics, and more recently, integrated into wildlife disease management. Cancer is a ubiquitous disease that affects most metazoan species; however, the role of oncogenic phenomena in eco‐evolutionary processes and its implications for wildlife management and conservation remains undeveloped. Despite the pervasive nature of cancer across taxa, our ability to detect its occurrence, progression and prevalence in wildlife populations is constrained due to logistic and diagnostic limitations, which suggests that most cancers in the wild are unreported and understudied. Nevertheless, an increasing number of virus‐associated and directly transmissible cancers in terrestrial and aquatic environments have been detected. Furthermore, anthropogenic activities and sudden environmental changes are increasingly associated with cancer incidence in wildlife. This highlights the need to upscale surveillance efforts, collection of critical data and developing novel approaches for studying the emergence and evolution of cancers in the wild. Here, we discuss the relevance of malignant cells as important agents of selection and offer a holistic framework to understand the interplay of ecological, epidemiological and evolutionary dynamics of cancer in wildlife. We use a directly transmissible cancer (devil facial tumour disease) as a model system to reveal the potential evolutionary dynamics and broader ecological effects of cancer epidemics in wildlife. We provide further examples of tumour–host interactions and trade‐offs that may lead to changes in life histories, and epidemiological and population dynamics. Within this framework, we explore immunological strategies at the individual level as well as transgenerational adaptations at the population level. Then, we highlight the need to integrate multiple disciplines to undertake comparative cancer research at the human–domestic–wildlife interface and their environments. Finally, we suggest strategies for screening cancer incidence in wildlife and discuss how to integrate ecological and evolutionary concepts in the management of current and future cancer epizootics.https://doi.org/10.1111/eva.12948cancerdisease ecologyhost–pathogen interactionsnatural selectiontransmissible tumourwildlife management