Ecological and Evolutionary Consequences of Anticancer Adaptations

Boutry, Justine; Dujon, Antoine; Gérard, Anne-Lise; Tissot, Sophie; MacDonald, Nick; Schultz, Aaron G.; Biro, Peter A.; Beckmann, Christa; Hamede, Rodrigo; Hamilton, David G.; Giraudeau, Mathieu; Újvári, Beáta; Thomas, Frédéric

doi:10.1016/j.isci.2020.101716

Cited by 11 publications

(12 citation statements)

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“…This especially applies to transmissible cancers, which can threaten the survival of species and raise the question of the extent to which they can be considered to be a separate species from their hosts (Russell et al, 2018). Just as with other animals, the evolution of humans was likely shaped by cancer (Boutry et al, 2020; Kang & Michalak, 2014; Thomas, Giraudeau, Renaud, et al, 2019). The environments in which humans now live and the associated lifestyle changes have undergone dramatic alterations since prehistoric times (Greaves & Aktipis, 2016).…”

Section: Introductionmentioning

confidence: 99%

Identifying key questions in the ecology and evolution of cancer

Dujon

Aktipis

Alix‐Panabières

et al. 2021

Evolutionary Applications

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The application of evolutionary and ecological principles to cancer prevention and treatment, as well as recognizing cancer as a selection force in nature, has gained impetus over the last 50 years. Following the initial theoretical approaches that combined knowledge from interdisciplinary fields, it became clear that using the eco-evolutionary framework is of key importance to understand cancer. We are now at a pivotal point where accumulating evidence starts to steer the future directions of the discipline and allows us to underpin the key challenges that remain to be addressed. Here, we aim to assess current advancements in the field and to suggest future directions for research.First, we summarize cancer research areas that, so far, have assimilated ecological and evolutionary principles into their approaches and illustrate their key importance. Then, we assembled 33 experts and identified 84 key questions, organized around nine major themes, to pave the foundations for research to come. We highlight the urgent need for broadening the portfolio of research directions to stimulate novel approaches at the interface of oncology and ecological and evolutionary sciences. We conclude that progressive and efficient cross-disciplinary collaborations that draw on the expertise of the fields of ecology, evolution and cancer are essential in order to efficiently address current and future questions about cancer. | INTRODUC TI ONThe application of evolutionary and ecological principles to preventing and treating cancer , as well as to understanding the impact of cancer on organismal health, fitness, species stability and ecosystem functioning (Thomas et al., 2017), has been gaining increasing attention and recognition among both oncologists and biologists since the seminal work of Cairns (1975), Nordling (1953 and Nowell (1976), more than 45 years ago. Most scientists today agree that this evolutionary view has deeply transformed the way we understand the biology of cancer-explaining its origin and the recrudescence of cancer cells as well as elucidating reasons for therapy failures. Following the theoretical development of a new interdisciplinary field that combines expertise from mathematicians, data scientists and biostatisticians, geneticists, evolutionary biologists, ecologists, physicists and oncologists, we are now at a pivotal point where empirical data and evidence are accumulating and guiding future directions of the discipline (Ujvari et al., 2017). We believe that the time has arrived to take stock of current advancements and to inform the course of future research. Cancer is a disease that impacts every country worldwide (18.1 million new cases and 9.6 million death in 2018; Bray et al., 2018), and these oncogenic processes are an inevitable phenomenon of metazoan life. Identifying the key questions in the ecology and evolution of cancer will provide a cornerstone in cancer and evolutionary research for the coming years. This will provide the basis for the development of efficient strategies to either preven...

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Section: Introductionmentioning

confidence: 99%

Identifying key questions in the ecology and evolution of cancer

Dujon

Aktipis

Alix‐Panabières

et al. 2021

Evolutionary Applications

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“…Potential examples are the placozoan Trichoplax adhaerens , which can tolerate levels of radiation of 248.6 Gy by overexpressing genes involved in DNA repair (Fortunato et al, 2021), or the planarians Girardia ( Dugesia ) tigrina and Polycelis feline which recover quickly from an acute sublethal exposure to ultraviolet radiation without developing cancer (Kalafatić et al, 2006). Such results are important to consider because they make it possible to explore trade‐offs between the ability of a species to repair its DNA, other damages leading to cancer, and the maintenance of other important functions such as movement or reproduction (Boutry et al, 2020; Dujon et al, 2022). The use of a positive control during such experiments can help identify such situations.…”

Section: Resultsmentioning

confidence: 99%

A review of the methods used to induce cancer in invertebrates to study its effects on the evolution of species and ecosystem functioning

et al. 2022

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“…Indeed, because sexual selection processes may be intense in natural populations depending on the ecological contexts, it could be expected that animals benefiting from abundant resources might develop secondary sexual traits whose expression level is higher than that corresponding to their cancer defenses. A rapid evolution in this direction would then drive genotypes away from the optimum, which would result in an increased risk of cancer, at least until the species or population adapts to the changes (Abegglen et al, 2015;Boutry et al, 2020). Such kind of mismatch scenario could potentially be investigated in habitat when wildlife artificially benefits from excessive quantity of food.…”

Section: Intra-sexual Selectionmentioning

confidence: 99%

Cancer Susceptibility as a Cost of Reproduction and Contributor to Life History Evolution

et al. 2022

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Reproduction is one of the most energetically demanding life-history stages. As a result, breeding individuals often experience trade-offs, where energy is diverted away from maintenance (cell repair, immune function) toward reproduction. While it is increasingly acknowledged that oncogenic processes are omnipresent, evolving and opportunistic entities in the bodies of metazoans, the associations among reproductive activities, energy expenditure, and the dynamics of malignant cells have rarely been studied. Here, we review the diverse ways in which age-specific reproductive performance (e.g., reproductive aging patterns) and cancer risks throughout the life course may be linked via trade-offs or other mechanisms, as well as discuss situations where trade-offs may not exist. We argue that the interactions between host–oncogenic processes should play a significant role in life-history theory, and suggest some avenues for future research.

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Ecological and Evolutionary Consequences of Anticancer Adaptations

Cited by 11 publications

References 153 publications

Identifying key questions in the ecology and evolution of cancer

Identifying key questions in the ecology and evolution of cancer

A review of the methods used to induce cancer in invertebrates to study its effects on the evolution of species and ecosystem functioning

Cancer Susceptibility as a Cost of Reproduction and Contributor to Life History Evolution

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