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 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.

Transmissible cancers in mammals and bivalves: How many examples are there?

“…This is especially true for virulent transmissible cancer lineages that can threaten already endangered wildlife populations (e.g., as in the Tasmanian devil [ 12,15 ] ) and cause changes in trophic cascades. [ 15,61 ] In addition to contributing to the conservation of those species, [ 19 ] obtaining insights on transmissible cancers in the wild may lead to new avenues to understand and treat human cancers. [ 62,63 ]…”

“…[ 2 ] In addition, apart from the fundamental information on the ecology and evolution of host‐tumour interactions, the knowledge generated here could help to predict and/or mitigate the effect of both transmissible or non‐transmissible cancers on animal populations and ecosystems. [ 19,20 ]…”

Darwin, the devil, and the management of transmissible cancers

“…While some cancerprotection adaptations are very old and phylogenetically well conserved, such as cancer-suppression mechanisms (Nunney 2013), others are species specific and shaped by ecological processes and life-history traits (Ujvari et al 2016). An increasing number of infectious cancers, virus associated and directly transmissible, are occurring in terrestrial and aquatic environments (Hamede et al 2020). Thus, cancer is nowadays regarded as a disease of conservation concern (McAloose & Newton 2009), particularly for threatened wildlife (Hamede at al.…”

“…An increasing number of infectious cancers, virus associated and directly transmissible, are occurring in terrestrial and aquatic environments (Hamede et al 2020). Thus, cancer is nowadays regarded as a disease of conservation concern (McAloose & Newton 2009), particularly for threatened wildlife (Hamede at al. 2020).…”

The interface between ecology, evolution, and cancer: More than ever a relevant research direction for both oncologists and ecologists

“…Thus, the coming years bring exciting opportunities for ecologists and evolutionary biologists to finally consider and accept oncobiota as a key player of the holobiont, and thus initiate and conduct theoretical and empirical research that adopts a very innovative perspective on the ecological and evolutionary importance of malignant cells. Using Tasmania devils and DFTD as a model system, Hamede et al (2020, This volume) discussed the relevance of cancer cells as selective agents and suggested a holistic framework to understand the interplay of ecological, epidemiological, and evolutionary dynamics of cancer in wildlife. Using a modeling approach, Perret, Gidoin, Ujvari, Thomas, and Roche (2020, This volume) explored, for the first time at the ecosystem level, the role of cancer in species interactions, notably host–predator interactions, and how in return, the outcome of alteredinterplay could affect the evolution of resistance mechanisms against cancer.…”