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1. Modeling of senescent cell dynamics predicts a late‐life decrease in cancer incidence

Author

Margaux Bieuville, Tazzio Tissot, Alexandre Robert, Pierre‐Yves Henry, and Samuel Pavard

Subjects
ageing, cancer, demography, evolution, life‐history traits, Peto's paradox, Evolution, QH359-425
Abstract

Abstract Current oncogenic theories state that tumors arise from cell lineages that sequentially accumulate (epi)mutations, progressively turning healthy cells into carcinogenic ones. While those models found some empirical support, they are little predictive of intraspecies age‐specific cancer incidence and of interspecies cancer prevalence. Notably, in humans and lab rodents, a deceleration (and sometimes decline) of cancer incidence rate has been found at old ages. Additionally, dominant theoretical models of oncogenesis predict that cancer risk should increase in large and/or long‐lived species, which is not supported by empirical data. Here, we explore the hypothesis that cellular senescence could explain those incongruent empirical patterns. More precisely, we hypothesize that there is a trade‐off between dying of cancer and of (other) ageing‐related causes. This trade‐off between organismal mortality components would be mediated, at the cellular scale, by the accumulation of senescent cells. In this framework, damaged cells can either undergo apoptosis or enter senescence. Apoptotic cells lead to compensatory proliferation, associated with an excess risk of cancer, whereas senescent cell accumulation leads to ageing‐related mortality. To test our framework, we build a deterministic model that first describes how cells get damaged, undergo apoptosis, or enter senescence. We then translate those cellular dynamics into a compound organismal survival metric also integrating life‐history traits. We address four different questions linked to our framework: can cellular senescence be adaptive, do the predictions of our model reflect epidemiological patterns observed among mammal species, what is the effect of species sizes on those answers, and what happens when senescent cells are removed? Importantly, we find that cellular senescence can optimize lifetime reproductive success. Moreover, we find that life‐history traits play an important role in shaping the cellular trade‐offs. Overall, we demonstrate that integrating cellular biology knowledge with eco‐evolutionary principles is crucial to solve parts of the cancer puzzle.

Published
2023
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2. Number of lifetime menses increases breast cancer occurrence in postmenopausal women at high familial risk

Author

Margaux Bieuville, Dominique Faugère, Virginie Galibert, Morgane Henard, Antoine M. Dujon, Beata Ujvari, Pascal Pujol, Benjamin Roche, and Frédéric Thomas

Subjects
evolutionary mismatch, breast cancer, reproductive pattern, survival models, menopause, Evolution, QH359-425, Ecology, QH540-549.5
Abstract

It is increasingly thought that part of human susceptibility to cancer is the result of evolutionary mismatches: our ancestors evolved cancer suppression mechanisms in a world largely different from our modern environments. In that context, it has been shown in cohorts from general Western populations that reproductive traits modulate breast cancer risk. Overall, the more menses women experience, the more at risk they are to develop postmenopausal breast cancer. This points towards an evolutionary mismatch but brings the question whether the reproductive pattern also modulates the breast cancer risk in menopausal women at high familial risk. We thus studied the influence of menses on breast cancer risk in a case–control study of 90 postmenopausal women (including BRCA1/2 and non BRCA1/2) nested within a cohort at high familial risk. We tested the association of the lifetime number of menses and the number of menses before first full-term pregnancy with postmenopausal breast cancer risk using Cox survival models. We showed that the total lifetime number of menses was significantly associated with postmenopausal breast cancer risk and associated with a quicker onset of breast cancer after menopause. Those results align with similar studies lead in general cohorts and suggest that the reproductive pattern modulates the familial risk of developing breast cancer after menopause. Altogether, those results impact how we envision breast cancer prevention and call for more research on how ecological and genetic factors shape breast cancer risk.

Published
2023
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3. Rare and unique adaptations to cancer in domesticated species: An untapped resource?

Author

Frédéric Thomas, Mathieu Giraudeau, Nolwenn M. Dheilly, Flora Gouzerh, Justine Boutry, Christa Beckmann, Peter A. Biro, Rodrigo Hamede, Jerome Abadie, Sophie Labrut, Margaux Bieuville, Dorothée Misse, Georgina Bramwell, Aaron Schultz, Guillaume Le Loc'h, Orsolya Vincze, Benjamin Roche, François Renaud, Tracey Russell, and Beata Ujvari

Subjects
cancer, domestication, domestication syndrome, evolution, evolutionary mismatch, selection, Evolution, QH359-425
Abstract

Abstract Strong and ongoing artificial selection in domestic animals has resulted in amazing phenotypic responses that benefit humans, but often at a cost to an animal's health, and problems related to inbreeding depression, including a higher incidence of cancer. Despite high rates of cancer in domesticated species, little attention has been devoted to exploring the hypothesis that persistent artificial selection may also favour the evolution of compensatory anticancer defences. Indeed, there is evidence for effective anti‐cancer defences found in several domesticated species associated with different cancer types. We also suggest that artificial selection can favour the “domestication” of inherited oncogenic mutations in rare instances, retaining those associated to late and/or less aggressive cancers, and that by studying these seemingly rare anticancer adaptations, novel cancer treatments may be found.

Published
2020
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4. Rare and unique adaptations to cancer in domesticated species: An untapped resource?

Author

Dorothée Missé, Georgina Bramwell, Aaron G. Schultz, Margaux Bieuville, Beata Ujvari, Nolwenn M. Dheilly, Jérôme Abadie, Péter Biró, Sophie Labrut, Tracey Russell, Flora Gouzerh, Justine Boutry, François Renaud, Orsolya Vincze, Rodrigo Hamede, Guillaume Le Loc'h, Mathieu Giraudeau, Benjamin Roche, Frédéric Thomas, Christa Beckmann, Centre de Recherches Ecologiques et Evolutives sur le Cancer (CREEC), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Interactions hôtes-agents pathogènes [Toulouse] (IHAP), Institut National de la Recherche Agronomique (INRA)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Unité de modélisation mathématique et informatique des systèmes complexes [Bondy] (UMMISCO), Institut de la francophonie pour l'informatique-Université Cheikh Anta Diop [Dakar, Sénégal] (UCAD)-Université Gaston Bergé (Saint-Louis, Sénégal)-Universtié Yaoundé 1 [Cameroun]-Université Cadi Ayyad [Marrakech] (UCA)-Sorbonne Université (SU)-Institut de Recherche pour le Développement (IRD [France-Nord]), Centre de Recherches Ecologiques et Evolutives sur le Cancer (MIVEGEC-CREEC), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), School of Marine and Atmospheric Sciences [Stony Brook] (SoMAS), Stony Brook University [SUNY] (SBU), State University of New York (SUNY)-State University of New York (SUNY), Deakin University, Burwood, Australia, Deakin University [Burwood], Western Sydney University, University of Tasmania [Hobart, Australia] (UTAS), Animaux modèles pour la recherche en oncologie comparée (AMaROC), Ecole Nationale Vétérinaire, Agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS), Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Hungarian Department of Biology and Ecology [Cluj‑Napoca, Romania], Babes-Bolyai University [Cluj-Napoca] (UBB), MTA Centre for Ecological Research [Tihany], Hungarian Academy of Sciences (MTA), Institut de Recherche pour le Développement (IRD [France-Nord])-Institut de la francophonie pour l'informatique-Université Cheikh Anta Diop [Dakar, Sénégal] (UCAD)-Université Gaston Bergé (Saint-Louis, Sénégal)-Université Cadi Ayyad [Marrakech] (UCA)-Université de Yaoundé I-Sorbonne Université (SU), The University of Sydney, This work was supported by an ARC Linkage (LP170101105), Deakin SEBE_RGS_2019, an ANR TRANSCAN (ANR-18-CE35-0009) and a CNRS 'International Associated Laboratory Grant.' Support was also provided by the Rotary Club Les Sables d’Olonne to FT. OV is supported by the Romanian Ministry of Research and Innovation (PN-III-P4-ID-PCE-2016-0404), by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences and by the New National Excellence Program of the Ministry of Innovation and Technology (ÚNKP-19-4-DE-538)., ANR-18-CE35-0009,TRANSCAN,ECOLOGIE ET EVOLUTION DES CANCERS TRANSMISSIBLES(2018), École nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), and Université de Yaoundé I-Institut de la francophonie pour l'informatique-Université Cheikh Anta Diop [Dakar, Sénégal] (UCAD)-Université Gaston Bergé (Saint-Louis, Sénégal)-Université Cadi Ayyad [Marrakech] (UCA)-Sorbonne Université (SU)-Institut de Recherche pour le Développement (IRD [France-Nord])

Subjects
0106 biological sciences, 0301 basic medicine, evolutionary mismatch, Resource (biology), [SDV]Life Sciences [q-bio], domestication syndrome, lcsh:Evolution, selection, Biology, 010603 evolutionary biology, 01 natural sciences, 03 medical and health sciences, domestication, evolutionary, evolution, Genetics, Inbreeding depression, medicine, lcsh:QH359-425, cancer, Domestication, Ecology, Evolution, Behavior and Systematics, Selection (genetic algorithm), High rate, Cancer, Mismatch theory, medicine.disease, 030104 developmental biology, Evolutionary biology, General Agricultural and Biological Sciences, mismatch
Abstract

International audience; Strong and ongoing artificial selection in domestic animals has resulted in amazing phenotypic responses that benefit humans, but often at a cost to an animal's health, and problems related to inbreeding depression, including a higher incidence of cancer. Despite high rates of cancer in domesticated species, little attention has been devoted to exploring the hypothesis that persistent artificial selection may also favour the evolution of compensatory anticancer defences. Indeed, there is evidence for effective anti‐cancer defences found in several domesticated species associated with different cancer types. We also suggest that artificial selection can favour the “domestication” of inherited oncogenic mutations in rare instances, retaining those associated to late and/or less aggressive cancers, and that by studying these seemingly rare anticancer adaptations, novel cancer treatments may be found.

Published
2020

5. Cancer risk across mammals

Author

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, Hungarian Department of Biology and Ecology [Cluj‑Napoca, Romania], Babes-Bolyai University [Cluj-Napoca] (UBB), Interdisciplinary Center on Population Dynamics, University of Southern Denmark (SDU), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Éco-Anthropologie (EAE), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS), Centre de Recherches Ecologiques et Evolutives sur le Cancer (MIVEGEC-CREEC), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM), Deakin University [Burwood], University of California [Santa Barbara] (UCSB), University of California, Arizona State University [Tempe] (ASU), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM), LIttoral ENvironnement et Sociétés (LIENSs), La Rochelle Université (ULR)-Centre National de la Recherche Scientifique (CNRS), Biodémographie évolutive, Département écologie évolutive [LBBE], Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Ecologie et évolution des populations, Éco-Anthropologie (EA), Universidad Nacional Autónoma de México = National Autonomous University of Mexico (UNAM), University of Bath [Bath], University of California [Santa Barbara] (UC Santa Barbara), University of California (UC), 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., and ANR-18-CE35-0009,TRANSCAN,ECOLOGIE ET EVOLUTION DES CANCERS TRANSMISSIBLES(2018)

Subjects
Aging, [SDV]Life Sciences [q-bio], Longevity, MESH: Carnivory, Species Specificity, Risk Factors, MESH: Risk Factors, Neoplasms, Animals, Body Size, MESH: Species Specificity, MESH: Aging, MESH: Animals, MESH: Neoplasms, MESH: Phylogeny, Phylogeny, Mammals, MESH: Mammals / classification, Multidisciplinary, MESH: Body Size, Body Weight, Carnivory, Diet, MESH: Body Weight, MESH: Diet / veterinary, MESH: Longevity, MESH: Aùimals, Zoo, Animals, Zoo
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.

Published
2022

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