Cancer risk across mammals

Orsolya Vincze, Fernando Colchero, Jean Francois Lemaître, Dalia A. Conde, Samuel Pavard, Margaux Bieuville, Araxi O. Urrutia, Beata Ujvari, Amy M. Boddy, Carlo C. Maley, Frédéric Thomas, Mathieu Giraudeau

Research output: Contribution to journalArticlepeer-review

116 Citations (SciVal)

Abstract

Cancer is a ubiquitous disease of metazoans, predicted to disproportionately affect larger, long-lived organisms owing to their greater number of cell divisions, and thus increased probability of somatic mutations1,2. While elevated cancer risk with larger body size and/or longevity has been documented within species3–5, Peto’s paradox indicates the apparent lack of such an association among taxa6. Yet, unequivocal empirical evidence for Peto’s paradox is lacking, stemming from the difficulty of estimating cancer risk in non-model species. Here we build and analyse a database on cancer-related mortality using data on adult zoo mammals (110,148 individuals, 191 species) and map age-controlled cancer mortality to the mammalian tree of life. We demonstrate the universality and high frequency of oncogenic phenomena in mammals and reveal substantial differences in cancer mortality across major mammalian orders. We show that the phylogenetic distribution of cancer mortality is associated with diet, with carnivorous mammals (especially mammal-consuming ones) facing the highest cancer-related mortality. Moreover, we provide unequivocal evidence for the body size and longevity components of Peto’s paradox by showing that cancer mortality risk is largely independent of both body mass and adult life expectancy across species. These results highlight the key role of life-history evolution in shaping cancer resistance and provide major advancements in the quest for natural anticancer defences.

Original languageEnglish
Pages (from-to)263-267
Number of pages5
JournalNature
Volume601
Issue number7892
Early online date22 Dec 2021
DOIs
Publication statusPublished - 13 Jan 2022

Bibliographical note

Funding Information:
Acknowledgements We are grateful to P. Bustamante and T. Székely for constructive criticism on an earlier version of the manuscript, and R. Thompson and A. Teare for invaluable explanations of ZIMS data. We are grateful to more than 1,200 zoo and aquarium members of Species360 that record data in ZIMS, making this study possible. O.V. was financed by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences and by the New National Excellence Programme of the Hungarian Ministry of Innovation and Technology. F.T. is supported by the MAVA Foundation, the ANR TRANSCAN (ANR-18-CE35-0009) and a CNRS International Associated Laboratory Grant. C.C.M. and A.M.B. were supported in part by NIH grant U54 CA217376. C.C.M. was also in part supported by NIH grant U2C CA233254, as well as CDMRP Breast Cancer Research Program Award BC132057 and the Arizona Biomedical Research Commission grant ADHS18-198847. D.A.C. was financed by the Species360 CSA sponsors: Copenhagen Zoo, Wildlife Reserves of Singapore and the World Association of Zoos and Aquariums. The findings, opinions and recommendations expressed here are those of the authors and not necessarily those of the universities where the research was performed or the United States National Institutes of Health.

Data availability
Data used for the analysis presented in the paper are available at https://
github.com/OrsolyaVincze/VinczeEtal2021Nature/blob/main/Supple
mentaryData.xls. Raw data used to estimate cancer risk (Species360
Data Use Approval Number 73836) cannot be publicly shared, as Species360 is the custodian (not the owner) of their members’ data. Raw data
are accessible through Research Request applications (form available at
https://docs.google.com/forms/d/1znoy62VEkDlhAp_0RfEvF7Zsx03g
4W5AlppJHqo3_WQ/viewform?edit_requested=true&pli=1). Research
Requests are reviewed by both the Species360 Research Committee and
their Board of Trustees every four months. The Board of Trustees makes
the final decision on data sharing, based on recommendations by the
Research Committee. Once Species360 grants access to data, they are
intended only for and restricted to use in the project they were approved
for and for a single publication. The researcher cannot use them for
other projects, publications and/or purposes, nor can the researcher
share the data with third parties. For any other inquires, all of the details
for the submission of research requests to Species360 can be found at
https://conservation.species360.org/wp-content/uploads/2020/08/
Species360-Sharing-Data-v3-3_komprimeret.pdf. Any email communications should be directed to [email protected].

Funding

Acknowledgements We are grateful to P. Bustamante and T. Székely for constructive criticism on an earlier version of the manuscript, and R. Thompson and A. Teare for invaluable explanations of ZIMS data. We are grateful to more than 1,200 zoo and aquarium members of Species360 that record data in ZIMS, making this study possible. O.V. was financed by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences and by the New National Excellence Programme of the Hungarian Ministry of Innovation and Technology. F.T. is supported by the MAVA Foundation, the ANR TRANSCAN (ANR-18-CE35-0009) and a CNRS International Associated Laboratory Grant. C.C.M. and A.M.B. were supported in part by NIH grant U54 CA217376. C.C.M. was also in part supported by NIH grant U2C CA233254, as well as CDMRP Breast Cancer Research Program Award BC132057 and the Arizona Biomedical Research Commission grant ADHS18-198847. D.A.C. was financed by the Species360 CSA sponsors: Copenhagen Zoo, Wildlife Reserves of Singapore and the World Association of Zoos and Aquariums. The findings, opinions and recommendations expressed here are those of the authors and not necessarily those of the universities where the research was performed or the United States National Institutes of Health.

ASJC Scopus subject areas

  • General

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