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

Rodrigo Hamede,Menna Jones,Antoine M Dujon,Rachel Owen,Mathieu Giraudeau,Sarah Peck,Benjamin Roche,Beata Ujvari,Hannah Siddle,Frédéric Thomas

doi:10.1111/eva.12948

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.

Highlights

Over the last two decades, significant efforts have been made to incorporate ecological and evolutionary principles to better understand the dynamics of wildlife diseases and their impact on wild populations (Galvani, 2003; Tompkins, Dunn, Smith, & Telfer, 2011; Vander Wal et al, 2014)
The discovery of eight transmissible cancers in the last 25 years suggests that (a) some species/environments might be susceptible to these type of cancers, (b) there is a relationship between environmental change/disturbance and emergence of transmissible cancers or (c) transmissible cancers may have been more common throughout the evolutionary history of multicellular species, but our ability to detect them has only recently improved due to advances in biotechnology and multidisciplinary efforts in surveying populations
As we look towards the future, there is a unique opportunity to integrate human, experimental and animal cancer research

Summary

Introduction

Over the last two decades, significant efforts have been made to incorporate ecological and evolutionary principles to better understand the dynamics of wildlife diseases and their impact on wild populations (Galvani, 2003; Tompkins, Dunn, Smith, & Telfer, 2011; Vander Wal et al, 2014). Tumour–host interactions and evolutionary processes between hosts and malignant cells will provide new insights into our understanding of how cancer defence mechanisms arise and evolve in nature (Nunney, 2013).

Results

Conclusion