Approaches and methods to study wildlife cancer.
One Health
cancer
cancer diagnostic
disease ecology
wildlife disease
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
27 Aug 2024
27 Aug 2024
Historique:
received:
05
12
2023
accepted:
23
04
2024
medline:
27
8
2024
pubmed:
27
8
2024
entrez:
27
8
2024
Statut:
aheadofprint
Résumé
The last few years have seen a surge of interest from field ecologists and evolutionary biologists to study neoplasia and cancer in wildlife. This contributes to the One Health Approach, which investigates health issues at the intersection of people, wild and domestic animals, together with their changing environments. Nonetheless, the emerging field of wildlife cancer is currently constrained by methodological limitations in detecting cancer using non-invasive sampling. In addition, the suspected differential susceptibility and resistance of species to cancer often make the choice of a unique model species difficult for field biologists. Here, we provide an overview of the importance of pursuing the study of cancer in non-model organisms and we review the currently available methods to detect, measure and quantify cancer in the wild, as well as the methodological limitations to be overcome to develop novel approaches inspired by diagnostic techniques used in human medicine. The methodology we propose here will help understand and hopefully fight this major disease by generating general knowledge about cancer, variation in its rates, tumour-suppressor mechanisms across species as well as its link to life history and physiological characters. Moreover, this is expected to provide key information about cancer in wildlife, which is a top priority due to the accelerated anthropogenic change in the past decades that might favour cancer progression in wild populations.
Identifiants
pubmed: 39189422
doi: 10.1111/1365-2656.14144
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : ANR COVER
ID : ANR-23-CE02-0019
Organisme : Chaire d'excellence 'Cancer et Biodiversité'
Organisme : National Scientific Research Fund
ID : OTKA K143421
Organisme : NIH HHS
ID : U54 CA217376
Pays : United States
Organisme : NIH HHS
ID : U2C CA233254
Pays : United States
Organisme : NIH HHS
ID : P01 CA91955
Pays : United States
Organisme : NIH HHS
ID : R01 CA140657
Pays : United States
Organisme : NIH HHS
ID : BC132057
Pays : United States
Organisme : Arizona Biomedical Research Commission
ID : ADHS18-198847
Organisme : Hoffmann Family
Organisme : Estonian Research Council
ID : PSG458
Organisme : Australian Research Council
ID : DE170101116
Organisme : Australian Research Council
ID : LP170101105
Organisme : PAPPIT-DGAPA-UNAM
ID : IN200920
Organisme : Natural Environment Research Council
ID : NE/P004121/1
Organisme : Royal Society Funding
ID : DH071902
Organisme : Royal Society Funding
ID : RG0870644
Organisme : Royal Society Funding
ID : RG080272
Organisme : European Union Horizon 2020 Research
ID : 765492
Organisme : National Institute of Cancer
Organisme : SIRIC Montpellier Cancer Grant
ID : INCa_Inserm_DGOS_12553
Organisme : ERA-NET
Organisme : ANR EVOSEXCAN : ANR-23-CE13-0007
Organisme : Fonds Euroṕeen de Dé veloppement Ré gional PO/FEDER/FSE 2014-2020 - Collectivit́e Territoriale de Martinique
ID : Conventionn°MQ0017449
Informations de copyright
© 2024 The Author(s). Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.
Références
Abegglen, L. M., Caulin, A. F., Chan, A., Lee, K., Robinson, R., Campbell, M. S., Kiso, W. K., Schmitt, D. L., Waddell, P. J., Bhaskara, S., Jensen, S. T., Maley, C. C., & Schiffman, J. D. (2015). Potential mechanisms for cancer resistance in elephants and comparative cellular response to DNA damage in humans. Journal of the American Medical Association, 314(17), 1850–1860. https://doi.org/10.1001/jama.2015.13134
Aguirre, A. A., & Spraker, T. R. (1996). Microscopic and ultra‐structural evidence of herpesvirus‐like virus in Hawaiian green turtles (Chelonia mydas) with fibropapillomatosis. Southwest Fisheries Center Administrative report H‐96‐06C, NOAA, Honolulu.
Aktipis, A. C., Boddy, A. M., Jansen, G., Hibner, U., Hochberg, M. E., Maley, C. C., & Wilkinson, G. S. (2015). Cancer across the tree of life: Cooperation and cheating in multicellularity. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1673), 20140219. https://doi.org/10.1098/rstb.2014.0219
Allott, E. H., & Hursting, S. D. (2015). Obesity and cancer: Mechanistic insights from transdisciplinary studies. Endocrine‐Related Cancer, 22(6), R365–R386. https://doi.org/10.1530/ERC‐15‐0400
Anisimov, V. N., Ukraintseva, S. V., & Yashin, A. I. (2005). Cancer in rodents: Does it tell us about cancer in humans? Nature Reviews Cancer, 5(10), 807–819. https://doi.org/10.1038/nrc1715
Baines, C., Lerebours, A., Thomas, F., Fort, J., Kreitsberg, R., Gentes, S., Meitern, R., Saks, L., Ujvari, B., Giraudeau, M., & Sepp, T. (2021). Linking pollution and cancer in aquatic environments: A review. Environment International, 149, 106391. https://doi.org/10.1016/j.envint.2021.106391
Baumann, P. C., & Harshbarger, J. C. (1995). Decline in liver neoplasms in wild brown bullhead catfish after coking plant closes and environmental PAHs plummet. Environmental Health Perspectives, 103(2), 168–170. https://doi.org/10.1289/ehp.95103168
Beckmann, J. P., & Lackey, C. W. (2008). Carnivores, urban landscapes, and longitudinal studies: A case history of black bears. Human‐Wildlife Conflicts, 2(2), 168–174.
Belov, K. (2011). The role of the major histocompatibility complex in the spread of contagious cancers. Mammalian Genome, 22, 83–90.
Belov, K. (2012). Contagious cancer: Lessons from the devil and the dog. BioEssays, 34(4), 285–292. https://doi.org/10.1002/bies.201100161
Black, J. J., Evans, E. D., Harshbarger, J. C., & Zeigel, R. F. (1982). Epizootic neoplasms in fishes from a lake polluted by copper mining wastes. Journal of the National Cancer Institute, 69(4), 915–926. https://doi.org/10.1093/jnci/69.4.915
Boddy, A. M., Abegglen, L. M., Pessier, A. P., Aktipis, A. C., Schiffman, J. D., Maley, C. C., & Witte, C. (2020). Lifetime cancer prevalence and life history traits in mammals. Evolution, Medicine, and Public Health, 2020(1), 187–195. https://doi.org/10.1093/EMPH/EOAA015
Boddy, A. M., Kokko, H., Breden, F., Wilkinson, G. S., & Aktipis, A. C. (2015). Cancer susceptibility and reproductive trade‐offs: A model of the evolution of cancer defences. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1673), 20140220. https://doi.org/10.1098/rstb.2014.0220
Bramwell, G., Schultz, A. G., Sherman, C. D. H., Giraudeau, M., Thomas, F., Ujvari, B., & Dujon, A. M. (2021). A review of the potential effects of climate change on disseminated neoplasia with an emphasis on efficient detection in marine bivalve populations. Science of the Total Environment, 775, 145134. https://doi.org/10.1016/j.scitotenv.2021.145134
Browning, H. M., Gulland, F. M. D., Hammond, J. A., Colegrove, K. M., & Hall, A. J. (2015). Common cancer in a wild animal: The California sea lion (Zalophus californianus) as an emerging model for carcinogenesis. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1673), 20140228. https://doi.org/10.1098/rstb.2014.0228
Bundy, J. G., Davey, M. P., & Viant, M. R. (2009). Environmental metabolomics: A critical review and future perspectives. Metabolomics, 5(1), 3–21. https://doi.org/10.1007/s11306‐008‐0152‐0
Carballal, M. J., Barber, B. J., Iglesias, D., & Villalba, A. (2015). Neoplastic diseases of marine bivalves. Journal of Invertebrate Pathology, 131, 83–106. https://doi.org/10.1016/j.jip.2015.06.004
Cayuela, H., Olgun, K., Angelini, C., Üzüm, N., Peyronel, O., Miaud, C., Avcı, A., Lemaitre, J.‐F., & Schmidt, B. R. (2019). Slow life‐history strategies are associated with negligible actuarial senescence in western Palaearctic salamanders. Proceedings of the Royal Society B: Biological Sciences, 286(1909), 20191498. https://doi.org/10.1098/rspb.2019.1498
Ceballos, G., Ehrlich, P. R., & Dirzo, R. (2017). Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proceedings of the National Academy of Sciences of the United States of America, 114(30), E6089–E6096. https://doi.org/10.1073/pnas.1704949114
Chaloupka, M., Balazs, G. H., & Work, T. M. (2009). Rise and fall over 26 years of a marine epizootic in Hawaiian green sea turtles. Journal of Wildlife Diseases, 45(4), 1138–1142. https://doi.org/10.7589/0090‐3558‐45.4.1138
Chaudhuri, A. A., Chabon, J. J., Lovejoy, A. F., Newman, A. M., Stehr, H., Azad, T. D., Khodadoust, M. S., Esfahani, M. S., Liu, C. L., Zhou, L., Scherer, F., Kurtz, D. M., Say, C., Carter, J. N., Merriott, D. J., Dudley, J. C., Binkley, M. S., Modlin, L., Padda, S. K., … Diehn, M. (2017). Early detection of molecular residual disease in localized lung cancer by circulating tumor DNA profiling. Cancer Discovery, 7(12), 1394–1403. https://doi.org/10.1158/2159‐8290.CD‐17‐0716
Cheynel, L., Lemaître, J.‐F., Gaillard, J.‐M., Rey, B., Bourgoin, G., Ferté, H., Jégo, M., Débias, F., Pellerin, M., Jacob, L., & Gilot‐Fromont, E. (2017). Immunosenescence patterns differ between populations but not between sexes in a long‐lived mammal. Scientific Reports, 7(1), 1–11. https://doi.org/10.1038/s41598‐017‐13686‐5
Chmielewska, M., Łosiewicz, K., Socha, P., Męcik‐Kronenberg, T., & Wąsowicz, K. (2013). The application of circulating tumor cells detecting methods in veterinary oncology. Polish Journal of Veterinary Sciences, 16(1), 141–151. https://doi.org/10.2478/pjvs‐2013‐0022
Civitello, D. J., Cohen, J., Fatima, H., Halstead, N. T., Liriano, J., McMahon, T. A., Ortega, C. N., Sauer, E. L., Sehgal, T., Young, S., & Rohr, J. R. (2015). Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United States of America, 112(28), 8667–8671. https://doi.org/10.1073/pnas.1506279112
Clutton‐Brock, T., & Sheldon, B. C. (2010). Individuals and populations: The role of long‐term, individual‐based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution, 25(10), 562–573. https://doi.org/10.1016/j.tree.2010.08.002
Compton, Z., Harris, V., Mellon, W., Rupp, S., Mallo, D., Kapsetaki, S. E., Wilmot, M., Kennington, R., Noble, K., Baciu, C., Ramirez, L., Peraza, A., Martins, B., Sudhakar, S., Aksoy, S., Furukawa, G., Vincze, O., Giraudeau, M., Duke, E. G., … Boddy, A. M. (2023). Cancer prevalence across vertebrates. Research Square. https://doi.org/10.21203/rs.3.rs‐3117313/v1
Conde, D. A., Flesness, N., Colchero, F., Jones, O. R., & Scheuerlein, A. (2011). An emerging role of zoos to conserve biodiversity. Science, 331(6023), 1390–1391. https://doi.org/10.1126/science.1200674
Conde, D. A., Staerk, J., Colchero, F., da Silva, R., Schöley, J., Maria Baden, H., Jouvet, L., Fa, J. E., Syed, H., Jongejans, E., Meiri, S., Gaillard, J. M., Chamberlain, S., Wilcken, J., Jones, O. R., Dahlgren, J. P., Steiner, U. K., Bland, L. M., Gomez‐Mestre, I., … Vaupel, J. W. (2019). Data gaps and opportunities for comparative and conservation biology. Proceedings of the National Academy of Sciences of the United States of America, 116(19), 9658–9664. https://doi.org/10.1073/pnas.1816367116
Cortés‐Hernández, L. E., Eslami‐S, Z., & Alix‐Panabières, C. (2020). Liquid biopsy to detect circulating tumor cells: Is it ready for a value proposition in laboratory medicine? The Journal of Applied Laboratory Medicine, 5(5), 1027–1037. https://doi.org/10.1093/jalm/jfaa115
Cristiano, S., Leal, A., Phallen, J., Fiksel, J., Adleff, V., Bruhm, D. C., Jensen, S. Ø., Medina, J. E., Hruban, C., White, J. R., Palsgrove, D. N., Niknafs, N., Anagnostou, V., Forde, P., Naidoo, J., Marrone, K., Brahmer, J., Woodward, B. D., Husain, H., … Velculescu, V. E. (2019). Genome‐wide cell‐free DNA fragmentation in patients with cancer. Nature, 570(7761), 385–389. https://doi.org/10.1038/s41586‐019‐1272‐6
Crowley, E., Di Nicolantonio, F., Loupakis, F., & Bardelli, A. (2013). Liquid biopsy: Monitoring cancer‐genetics in the blood. Nature Reviews Clinical Oncology, 10(8), 472–484. https://doi.org/10.1038/nrclinonc.2013.110
Davey, G. (2007). Visitors' effects on the welfare of animals in the zoo: A review. Journal of Applied Animal Welfare Science, 10(2), 169–183. https://doi.org/10.1080/10888700701313595
DeBerardinis, R. J. (2008). Is cancer a disease of abnormal cellular metabolism? New angles on an old idea. Genetics in Medicine, 10(11), 767–777. https://doi.org/10.1097/GIM.0b013e31818b0d9b
DeGregori, J. (2011). Evolved tumor suppression: Why are we so good at not getting cancer? Cancer Research, 71(11), 3739–3744. https://doi.org/10.1158/0008‐5472.CAN‐11‐0342
Dela Cruz, F. N. D., Jr., Giannitti, F., Li, L., Woods, L. W., Del Valle, L., Delwart, E., & Pesavento, P. A. (2013). Novel polyomavirus associated with brain tumors in free‐ranging raccoons, western United States. Emerging Infectious Diseases, 19(1), 77–84.
Delaney, M. A., Ward, J. M., Walsh, T. F., Chinnadurai, S. K., Kerns, K., Kinsel, M. J., & Treuting, P. M. (2016). Initial case reports of cancer in naked mole‐rats (Heterocephalus glaber). Veterinary Pathology, 53(3), 691–696. https://doi.org/10.1177/0300985816630796
Destoumieux‐Garzón, D., Mavingui, P., Boetsch, G., Boissier, J., Darriet, F., Duboz, P., … Voituron, Y. (2018). The One Health concept: 10 years old and a long road ahead. Frontiers in Veterinary Science, 5, 14.
Dujon, A., Brown, J. S., Destoumieux‐Garzón, D., Vittecoq, M., Hamede, R., Tasiemski, A., Boutry, J., Tissot, S., Alix‐Panabieres, C., Pujol, P., Renaud, F., Simard, F., Roche, B., Ujvari, B., & Thomas, F. (2021). On the need for integrating cancer into the One Health perspective. Evolutionary Applications, 14(11), 2571–2575. https://doi.org/10.1111/eva.13303
Dujon, A. M., Bramwell, G., Roche, B., Thomas, F., & Ujvari, B. (2020). Transmissible cancers in mammals and bivalves: How many examples are there? BioEssays, 2000222. https://doi.org/10.1002/bies.202000222
Dujon, A. M., Gatenby, R. A., Bramwell, G., MacDonald, N., Dohrmann, E., Raven, N., Schultz, A., Hamede, R., Gérard, A. L., Giraudeau, M., Thomas, F., & Ujvari, B. (2020). Transmissible cancers in an evolutionary perspective. iScience, 23(7), 101269. https://doi.org/10.1016/j.isci.2020.101269
Dujon, A. M., Schofield, G., Bramwell, G., Raven, N., Hamede, R., Thomas, F., & Ujvari, B. (2020). Global meta‐analysis of over 50 years of multidisciplinary and international collaborations on transmissible cancers. Evolutionary Applications, 13(7), 1745–1755. https://doi.org/10.1111/eva.12938
Easton, D. F., Bishop, D. T., Ford, D., Crockford, G. P., Haites, N., Milner, B., Allan, L., King, M. C., Bowcock, A., Anderson, L., Easton, D. F., Ponder, B. A. J., Peto, J., Smith, S., Anderson, K., Ford, D., Stratton, M., Sobol, H., & Mazoyer, S. (1993). Genetic linkage analysis in familial breast and ovarian cancer: Results from 214 families. American Journal of Human Genetics, 52(4), 678–701.
Frankham, R. (2005). Genetics and extinction. Biological Conservation, 126(2), 131–140. https://doi.org/10.1016/j.biocon.2005.05.002
Gaillard, J.‐M., Lemaître, J.‐F., Berger, V., Bonenfant, C., Devillard, S., Douhard, M., Gamelon, M., Plard, F., & Lebreton, J. D. (2016). Life histories, axes of variation in. In The encyclopedia of evolutionary biology (pp. 312–323). Elsevier, Academic Press. https://hal‐univ‐lyon1.archives‐ouvertes.fr/hal‐02099457
Ganguly, B., Das, U., & Das, A. K. (2016). Canine transmissible venereal tumour: A review. Veterinary and Comparative Oncology, 14(1), 1–12. https://doi.org/10.1111/vco.12060
Gauthier, J. M., Dubeau, H., Rassart, E., Jarman, W. M., & Wells, R. S. (1999). Biomarkers of DNA damage in marine mammals. Mutation Research, Genetic Toxicology and Environmental Mutagenesis, 444(2), 427–439.
Giraudeau, M., Sepp, T., Ujvari, B., Ewald, P. W., & Thomas, F. (2018). Human activities might influence oncogenic processes in wild animal populations. Nature Ecology & Evolution, 2(7), 1065–1070. https://doi.org/10.1038/s41559‐018‐0558‐7
Giraudeau, M., Watson, H., Powell, D., Vincze, O., Thomas, F., Sepp, T., Ujvari, B., Le Loc'h, G., & Isaksson, C. (2020). Will urbanisation affect the expression level of genes related to cancer of wild great tits? Science of the Total Environment, 714, 135793. https://doi.org/10.1016/j.scitotenv.2019.135793
Gorbunova, V., Seluanov, A., Zhang, Z., Gladyshev, V. N., & Vijg, J. (2014). Comparative genetics of longevity and cancer: Insights from long‐lived rodents. Nature Reviews Genetics, 15(8), 531–540. https://doi.org/10.1038/nrg3728
Greaves, M. (2015). Evolutionary determinants of cancer. Cancer Discovery, 5(8), 806–820.
Greaves, M., & Aktipis, A. C. (2016). Mismatches with our ancestral environments and cancer risk. In C. C. Maley & M. Greaves (Eds.), Frontiers in cancer research: Evolutionary foundations, revolutionary directions (pp. 195–215). New York: Springer Verlag. https://doi.org/10.1007/978‐1‐4939‐6460‐4_10
Griffin, J. L., & Kauppinen, R. A. (2007). Tumour metabolomics in animal models of human cancer. Journal of Proteome Research, 6(2), 498–505. https://doi.org/10.1021/pr060464h
Grogan, K. E., Sauther, M. L., Cuozzo, F. P., & Drea, C. M. (2017). Genetic wealth, population health: Major histocompatibility complex variation in captive and wild ring‐tailed lemurs (Lemur catta). Ecology and Evolution, 7(19), 7638–7649. https://doi.org/10.1002/ece3.3317
Guerrero, R. B., Batts, K. P., Brandhagen, D. J., Germer, J. J., Perez, R. G., & Persing, D. H. (1997). Effects of formalin fixation and prolonged block storage on detection of hepatitis C virus RNA in liver tissue. Diagnostic Molecular Pathology: The American Journal of Surgical Pathology: Part B, 6(5), 277–281.
Habli, Z., AlChamaa, W., Saab, R., Kadara, H., & Khraiche, M. L. (2020). Circulating tumor cell detection technologies and clinical utility: Challenges and opportunities. Cancers, 12(7), 1930.
Hamede, R., Owen, R., Siddle, H., Peck, S., Jones, M., Dujon, A. M., Giraudeau, M., Roche, B., Ujvari, B., & Thomas, F. (2020). The ecology and evolution of wildlife cancers: Applications for management and conservation. Evolutionary Applications, 13(7), 1719–1732. https://doi.org/10.1111/eva.12948
Hammel, M., Touchard, F., Burioli, E. A. V., Paradis, L., Cerqueira, F., Chailler, E., Bernard, I., Cochet, H., Simon, A., Thomas, F., Destoumieux‐Garzón, D., Charrière, G. M., & Bierne, N. (2017). Marine transmissible cancer navigates urbanized waters, threatening spillover. Proceedings: Biological Sciences, 291(2017), 20232541. https://doi.org/10.1098/rspb.2023.2541
Hammer, A. S., Williams, B., Dietz, H. H., & Hamilton‐Dutoit, S. J. (2007). High‐throughput immunophenotyping of 43 ferret lymphomas using tissue microarray technology. Veterinary Pathology, 44(2), 196–203. https://doi.org/10.1354/vp.44‐2‐196
Haslam, D. W., & James, W. P. T. (2005). Obesity. The Lancet, 366, 1197–1209.
Hawkins, C. E., Baars, C., Hesterman, H., Hocking, G. J., Jones, M. E., Lazenby, B., Mann, D., Mooney, N., Pemberton, D., Pyecroft, S., Restani, M., & Wiersma, J. (2006). Emerging disease and population decline of an Island endemic, the Tasmanian devil Sarcophilus harrisii. Biological Conservation, 131(2), 307–324. https://doi.org/10.1016/j.biocon.2006.04.010
Healy, K., Ezard, T. H. G., Jones, O. R., Salguero‐Gómez, R., & Buckley, Y. M. (2019). Animal life history is shaped by the pace of life and the distribution of age‐specific mortality and reproduction. Nature Ecology & Evolution, 3(8), 1217–1224. https://doi.org/10.1038/s41559‐019‐0938‐7
Hollings, T., Jones, M., Mooney, N., & McCallum, H. (2016). Disease‐induced decline of an apex predator drives invasive dominated states and threatens biodiversity. Ecology, 97(2), 394–405. https://doi.org/10.1890/15‐0204.1
Iacobuzio‐Donahue, C. A., Michael, C., Baez, P., Kappagantula, R., Hooper, J. E., & Hollman, T. J. (2019). Cancer biology as revealed by the research autopsy. Nature Reviews Cancer, 19(12), 686–697. https://doi.org/10.1038/s41568‐019‐0199‐4
Jacqueline, C., Biro, P. A., Beckmann, C., Moller, A. P., Renaud, F., Sorci, G., Tasiemski, A., Ujvari, B., & Thomas, F. (2017). Cancer: A disease at the crossroads of trade‐offs. Evolutionary Applications, 10(3), 215–225. https://doi.org/10.1111/eva.12444
Karu, N., Wilson, R., Hamede, R., Jones, M., Woods, G. M., Hilder, E. F., & Shellie, R. A. (2016). Discovery of biomarkers for Tasmanian devil cancer (DFTD) by metabolic profiling of serum. Journal of Proteome Research, 15(10), 3827–3840. https://doi.org/10.1021/acs.jproteome.6b00629
Kataoka, C., & Kashiwada, S. (2021). Ecological risks due to immunotoxicological effects on aquatic organisms. International Journal of Molecular Sciences, 22(15), 8305.
Kato, S., Lippman, S. M., Flaherty, K. T., & Kurzrock, R. (2016). The conundrum of genetic “drivers” in benign conditions. Journal of the National Cancer Institute, 108(8), djw036. https://doi.org/10.1093/jnci/djw036
Kaushik, A. K., & DeBerardinis, R. J. (2018). Applications of metabolomics to study cancer metabolism. Biochimica et Biophysica Acta, Reviews on Cancer, 1870(1), 2–14. https://doi.org/10.1016/j.bbcan.2018.04.009
Keane, M., Semeiks, J., Webb, A. E., Li, Y. I., Quesada, V., Craig, T., Madsen, L. B., van Dam, S., Brawand, D., Marques, P. I., Michalak, P., Kang, L., Bhak, J., Yim, H. S., Grishin, N. V., Nielsen, N. H., Heide‐Jørgensen, M. P., Oziolor, E. M., Matson, C. W., … deMagalhães, J. P. (2015). Insights into the evolution of longevity from the bowhead whale genome. Cell Reports, 10(1), 112–122. https://doi.org/10.1016/j.celrep.2014.12.008
King, D. P., Hure, M. C., Goldstein, T., Aldridge, B. M., Gulland, F. M., Saliki, J. T., … Stott, J. L. (2002). Otarine herpesvirus‐1: A novel gammaherpesvirus associated with urogenital carcinoma in California sea lions (Zalophus californianus). Veterinary Microbiology, 86(1–2), 131–137.
Klimentidis, Y. C., Beasley, T. M., Lin, H.‐Y., Murati, G., Glass, G. E., Guyton, M., Newton, W., Jorgensen, M., Heymsfield, S. B., Kemnitz, J., Fairbanks, L., & Allison, D. B. (2011). Canaries in the coal mine: A cross‐species analysis of the plurality of obesity epidemics. Proceedings of the Royal Society B: Biological Sciences, 278(1712), 1626–1632. https://doi.org/10.1098/rspb.2010.1890
Kuiken, T., Ryser‐Degiorgis, M. P., Gavier‐Widen, D., & Gortazar, C. (2011). Establishing a European network for wildlife health surveillance. Revue Scientifique et Technique de l'OIE, 30(3), 755–761. https://doi.org/10.20506/rst.30.3.2067
LaConti, J. J., Laiakis, E. C., Mays, D. D., Peran, I., Kim, S. E., Shay, J. W., Riegel, A. T., Fornace, A. J., & Wellstein, A. (2015). Distinct serum metabolomics profiles associated with malignant progression in the KrasG12D mouse model of pancreatic ductal adenocarcinoma. BMC Genomics, 16(1), 1–10. https://doi.org/10.1186/1471‐2164‐16‐S1‐S1
Lemaître, J.‐F., Pavard, S., Giraudeau, M., Vincze, O., Jennings, G., Hamede, R., Ujvari, B., & Thomas, F. (2020). Eco‐evolutionary perspectives of the dynamic relationships linking senescence and cancer. Functional Ecology, 34(1), 141–152. https://doi.org/10.1111/1365‐2435.13394
Lerebours, A., Cambier, S., Hislop, L., Adam‐Guillermin, C., & Bourdineaud, J. P. (2013). Genotoxic effects of exposure to waterborne uranium, dietary methylmercury and hyperoxia in zebrafish assessed by the quantitative RAPD‐PCR method. Mutation Research, Genetic Toxicology and Environmental Mutagenesis, 755(1), 55–60.
Lerebours, A., Stentiford, G. D., Lyons, B. P., Bignell, J. P., Derocles, S. A. P., & Rotchell, J. M. (2014). Genetic alterations and cancer formation in a European flatfish at sites of different contaminant burdens. Environmental Science and Technology, 48(17), 10448–10455. https://doi.org/10.1021/es502591p
Leroi, A. M., Koufopanou, V., & Burt, A. (2003). Cancer selection. Nature Reviews Cancer, 3(3), 226–231. https://doi.org/10.1038/nrc1016
Liu, M. C., Oxnard, G. R., Klein, E. A., Swanton, C., Seiden, M. V., Liu, M. C., Oxnard, G. R., Klein, E. A., Smith, D., Richards, D., Yeatman, T. J., Cohn, A. L., Lapham, R., Clement, J., Parker, A. S., Tummala, M. K., McIntyre, K., Sekeres, M. A., Bryce, A. H., … Berry, D. A. (2020). Sensitive and specific multi‐cancer detection and localization using methylation signatures in cell‐free DNA. Annals of Oncology, 31(6), 745–759. https://doi.org/10.1016/j.annonc.2020.02.011
Madsen, T., Arnal, A., Vittecoq, M., Bernex, F., Abadie, J., Labrut, S., Garcia, D., Faugère, D., Lemberger, K., Beckmann, C., Roche, B., Thomas, F., & Ujvari, B. (2017). Cancer prevalence and etiology in wild and captive animals. In Ecology and evolution of cancer (pp. 11–46). Academic Press. https://doi.org/10.1016/B978‐0‐12‐804310‐3.00002‐8
Manov, I., Hirsh, M., Iancu, T. C., Malik, A., Sotnichenko, N., Band, M., Avivi, A., & Shams, I. (2013). Pronounced cancer resistance in a subterranean rodent, the blind mole‐rat, Spalax: In vivo and in vitro evidence. BMC Biology, 11(1), 91. https://doi.org/10.1186/1741‐7007‐11‐91
Marconato, L., Facchinetti, A., Zanardello, C., Rossi, E., Vidotto, R., Capello, K., … Vascellari, M. (2019). Detection and prognostic relevance of circulating and disseminated tumour cell in dogs with metastatic mammary carcinoma: A pilot study. Cancers, 11(2), 163.
Maréchal, L., Semple, S., Majolo, B., & MacLarnon, A. (2016). Assessing the effects of tourist provisioning on the health of wild barbary macaques in Morocco. PLoS One, 11(5), e0155920. https://doi.org/10.1371/journal.pone.0155920
Martineau, D., Lemberger, K., Dallaire, A., Labelle, P., Lipscomb, T. P., Michel, P., & Mikaelian, I. (2002). Cancer in wildlife, a case study: Beluga from the St. Lawrence estuary, Québec, Canada. Environmental Health Perspectives, 110(3), 285–292. https://doi.org/10.1289/ehp.02110285
McAloose, D., & Newton, A. L. (2009). Wildlife cancer: A conservation perspective. Nature Reviews Cancer, 9(7), 517–526. https://doi.org/10.1038/nrc2665
McCallum, H., Jones, M., Hawkins, C., Hamede, R., Lachish, S., Sinn, D. L., Beeton, N., & Lazenby, B. (2009). Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease‐induced extinction. Ecology, 90(12), 3379–3392. https://doi.org/10.1890/08‐1763.1
Meitern, R., Fort, J., Giraudeau, M., Rattiste, K., Sild, E., & Sepp, T. (2020). Age‐dependent expression of cancer‐related genes in a long‐lived seabird. Evolutionary Applications, 13(7), 1708–1718. https://doi.org/10.1111/eva.13024
Merker, J. D., Oxnard, G. R., Compton, C., Diehn, M., Hurley, P., Lazar, A. J., Lindeman, N., Lockwood, C. M., Rai, A. J., Schilsky, R. L., Tsimberidou, A. M., Vasalos, P., Billman, B. L., Oliver, T. K., Bruinooge, S. S., Hayes, D. F., & Turner, N. C. (2018). Circulating tumor DNA analysis in patients with cancer: American society of clinical oncology and college of American pathologists joint review. Archives of Pathology and Laboratory Medicine, 142(10), 1242–1253. https://doi.org/10.5858/arpa.2018‐0901‐SA
Miller, M. G. (2007). Environmental metabolomics: A SWOT analysis (strengths, weaknesses, opportunities, and threats). Journal of Proteome Research, 6(2), 540–545. https://doi.org/10.1021/pr060623x
Miller, R. A., Harper, J. M., Dysko, R. C., Durkee, S. J., & Austad, S. N. (2002). Longer life spans and delayed maturation in wild‐derived mice. Experimental Biology and Medicine, 227(7), 500–508. https://doi.org/10.1177/153537020222700715
Moeller, R. B., Kalasinsky, V. F., Razzaque, M., Centeno, J. A., Dick, E. J., Abdal, M., Petrov, I. I., Dewitt, T. W., Al‐Attar, M., Pletcher, J. M., & Briskey, E. J. (1994). Assessment of the histopathological lesions and chemical analysis of feral cats to the smoke from the Kuwait oil fires. Journal of Environmental Pathology, Toxicology and Oncology, 13(2), 137–149. https://europepmc.org/article/med/7884645
Morgan, K. N., & Tromborg, C. T. (2007). Sources of stress in captivity. Applied Animal Behaviour Science, 102(3–4), 262–302. https://doi.org/10.1016/j.applanim.2006.05.032
Munson, L., & Moresco, A. (2007). Comparative pathology of mammary gland cancers in domestic and wild animals. Breast Disease, 28(1), 7–21. https://doi.org/10.3233/BD‐2007‐28102
Murray, M. H., Becker, D. J., Hall, R. J., & Hernandez, S. M. (2016). Wildlife health and supplemental feeding: A review and management recommendations. Biological Conservation, 204, 163–174. https://doi.org/10.1016/j.biocon.2016.10.034
Nunney, L. (2013). The real war on cancer: The evolutionary dynamics of cancer suppression. Evolutionary Applications, 6(1), 11–19. https://doi.org/10.1111/eva.12018
Nunney, L., Maley, C. C., Breen, M., Hochberg, M. E., & Schiffman, J. D. (2015). Peto's paradox and the promise of comparative oncology. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1673), 20140177. https://doi.org/10.1098/rstb.2014.0177
Odintsova, N. A. (2020). Leukemia‐like cancer in bivalves 1. Russian Journal of Marine Biology, 46(2), 59–67. https://doi.org/10.1134/S1063074020020078
Ohta, T. (1973). Slightly deleterious mutant substitutions in evolution. Nature, 246(5428), 96–98. https://doi.org/10.1038/246096a0
Oliveira Ribeiro, C. A., Vollaire, Y., Sanchez‐Chardi, A., & Roche, H. (2005). Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquatic Toxicology, 74(1), 53–69. https://doi.org/10.1016/j.aquatox.2005.04.008
Pantel, K., & Alix‐Panabières, C. (2019). Liquid biopsy and minimal residual disease — Latest advances and implications for cure. Nature Reviews Clinical Oncology, 16(7), 409–424. https://doi.org/10.1038/s41571‐019‐0187‐3
Peluc, S. I., Reed, W. L., McGraw, K. J., & Gibbs, P. (2012). Carotenoid supplementation and GnRH challenges influence female endocrine physiology, immune function, and egg‐yolk characteristics in Japanese quail (Coturnix japonica). Journal of Comparative Physiology B, 182(5), 687–702. https://doi.org/10.1007/s00360‐011‐0638‐3
Perlman, R. L. (2016). Mouse models of human disease: An evolutionary perspective. Evolution, medicine, and public. Evolution, Medicine, and Public Health, 2016(1), eow014. https://doi.org/10.1093/emph/eow014
Pesavento, P. A., Agnew, D., Keel, M. K., & Woolard, K. D. (2018). Cancer in wildlife: Patterns of emergence. Nature Reviews Cancer, 18(10), 646–661. https://doi.org/10.1038/s41568‐018‐0045‐0
Peters, R. H. (1983). The ecological implications of body size. Cambridge University Press. https://doi.org/10.1017/cbo9780511608551
Pewsner, M., Origgi, F. C., Frey, J., & Ryser‐Degiorgis, M.‐P. (2017). Assessing fifty years of general health surveillance of roe deer in Switzerland: A retrospective analysis of necropsy reports. PLoS One, 12(1), e0170338. https://doi.org/10.1371/journal.pone.0170338
Peyre, M., Vourc'h, G., Lefrançois, T., Martin‐Prevel, Y., Soussana, J. F., & Roche, B. (2021). PREZODE: Preventing zoonotic disease emergence. The Lancet, 397(10276), 792–793. https://doi.org/10.1016/S0140‐6736(21)00265‐8
Pierotti, R. J., & Fogg, B. R. (2017). The first domestication: How wolves and humans coevolved (Vol. 192). Yale University Press.
Pollock, R. E., & Roth, J. A. (1989). Cancer‐induced immunosuppression: Implications for therapy? Seminars in Surgical Oncology, 5(6), 414–419. https://doi.org/10.1002/ssu.2980050607
Pye, R. J., Pemberton, D., Tovar, C., Tubio, J. M. C., Dun, K. A., Fox, S., Darby, J., Hayes, D., Knowles, G. W., Kreiss, A., Siddle, H. V. T., Swift, K., Lyons, A. B., Murchison, E. P., & Woods, G. M. (2016). A second transmissible cancer in Tasmanian devils. Proceedings of the National Academy of Sciences of the United States of America, 113(2), 374–379. https://doi.org/10.1073/pnas.1519691113
Ramos‐Vara, J. A., Kiupel, M., Baszler, T., Bliven, L., Brodersen, B., Chelack, B., Czub, S., Del Piero, F., Dial, S., Ehrhart, E. J., Graham, T., Manning, L., Paulsen, D., Valli, V. E., & West, K. (2008). Suggested guidelines for immunohistochemical techniques in veterinary diagnostic laboratories. Journal of Veterinary Diagnostic Investigation, 20(4), 393–413.
Reinke, B. A., Miller, D. A., & Janzen, F. J. (2019). What have long‐term field studies taught us about population dynamics? Annual Review of Ecology, Evolution, and Systematics, 50, 261–278.
Rhee, J. S., Yu, I. T., Kim, B. M., Jeong, C. B., Lee, K. W., Kim, M. J., Lee, S.‐J., Park, G. S., & Lee, J.‐S. (2013). Copper induces apoptotic cell death through reactive oxygen species‐triggered oxidative stress in the intertidal copepod Tigriopus japonicus. Aquatic Toxicology, 132, 182–189.
Romano, F. R., Heinze, C. R., Barber, L. G., Mason, J. B., & Freeman, L. M. (2016). Association between body condition score and cancer prognosis in dogs with lymphoma and osteosarcoma. Journal of Veterinary Internal Medicine, 30(4), 1179–1186. https://doi.org/10.1111/jvim.13965
Sakurai, T., Kobayashi, J., Imaizumi, Y., & Suzuki, N. (2009). Non‐food‐chain transfer of sediment‐associated persistent organic pollutants to a marine benthic fish. Marine Pollution Bulletin, 58(7), 1072–1077. https://doi.org/10.1016/j.marpolbul.2009.04.009
Schulte‐Hostedde, A. I., Mazal, Z., Jardine, C. M., & Gagnon, J. (2018). Enhanced access to anthropogenic food waste is related to hyperglycemia in raccoons (Procyon lotor). Conservation Physiology, 6(1), coy026. https://doi.org/10.1093/conphys/coy026
Seluanov, A., Gladyshev, V. N., Vijg, J., & Gorbunova, V. (2018). Mechanisms of cancer resistance in long‐lived mammals. Nature Reviews Cancer, 18(7), 433–441. https://doi.org/10.1038/s41568‐018‐0004‐9
Sepp, T., McGraw, K. J., Kaasik, A., & Giraudeau, M. (2018). A review of urban impacts on avian life‐history evolution: Does city living lead to slower pace of life? Global Change Biology, 24(4), 1452–1469. https://doi.org/10.1111/gcb.13969
Sepp, T., Ujvari, B., Ewald, P. W., Thomas, F., & Giraudeau, M. (2019). Urban environment and cancer in wildlife: Available evidence and future research avenues. Proceedings of the Royal Society B: Biological Sciences, 286(1894), 20182434. https://doi.org/10.1098/rspb.2018.2434
Serkova, N. J., & Glunde, K. (2009). Metabolomics of cancer. Methods in Molecular Biology, 520, 273–295. https://doi.org/10.1007/978‐1‐60327‐811‐9_20
Sheldon, B. C., Kruuk, L. E., & Alberts, S. C. (2022). The expanding value of long‐term studies of individuals in the wild. Nature Ecology & Evolution, 6, 1799–1801. https://doi.org/10.1038/s41559‐022‐01940‐7
Stammnitz, M. R., Coorens, T. H. H., Gori, K. C., Hayes, D., Fu, B., Wang, J., Martin‐Herranz, D. E., Alexandrov, L. B., Baez‐Ortega, A., Barthorpe, S., Beck, A., Giordano, F., Knowles, G. W., Kwon, Y. M., Hall, G., Price, S., Pye, R. J., Tubio, J. M. C., Siddle, H. V. T., … Murchison, E. P. (2018). The origins and vulnerabilities of two transmissible cancers in tasmanian devils. Cancer Cell, 33(4), 607–619. https://doi.org/10.1016/j.ccell.2018.03.013
Stearns, S. C. (1983). The influence of size and phylogeny on patterns of covariation among life‐history traits in the mammals. Oikos, 41(2), 173–187. https://doi.org/10.2307/3544261
Sulak, M., Fong, L., Mika, K., Chigurupati, S., Yon, L., Mongan, N. P., Emes, R. D., & Lynch, V. J. (2016). TP53 copy number expansion is associated with the evolution of increased body size and an enhanced DNA damage response in elephants. eLife, 5, e11994. https://doi.org/10.7554/eLife.11994
Sunila, I., & Farley, C. A. (1989). Environmental limits for survival of sarcoma cells from the soft‐shell clam Mya arenaria. Diseases of Aquatic Organisms, 7, 111–115.
Thomas, F., Giraudeau, M., Dheilly, N. M., Gouzerh, F., Boutry, J., Beckmann, C., Biro, P. A., Hamede, R., Abadie, J., Labrut, S., Bieuville, M., Misse, D., Bramwell, G., Schultz, A., Le Loc'h, G., Vincze, O., Roche, B., Renaud, F., Russell, T., & Ujvari, B. (2020). Rare and unique adaptations to cancer in domesticated species: An untapped resource? Evolutionary Applications, 13(7), 1605–1614. https://doi.org/10.1111/eva.12920
Thomas, F., Giraudeau, M., Renaud, F., Ujvari, B., Roche, B., Pujol, P., Raymond, M., Lemaitre, J. F., & Alvergne, A. (2019). Can postfertile life stages evolve as an anticancer mechanism? PLoS Biology, 17(12), e3000565. https://doi.org/10.1371/journal.pbio.3000565
Thomas, F., Jacqueline, C., Tissot, T., Henard, M., Blanchet, S., Loot, G., Dawson, E., Mery, F., Renaud, F., Montagne, J., Beckmann, C., Biro, P. A., Hamede, R., & Ujvari, B. (2017). The importance of cancer cells for animal evolutionary ecology. Nature Ecology & Evolution, 1(11), 1592–1595. https://doi.org/10.1038/s41559‐017‐0343‐z
Tian, X., Azpurua, J., Hine, C., Vaidya, A., Myakishev‐Rempel, M., Ablaeva, J., Mao, Z., Nevo, E., Gorbunova, V., & Seluanov, A. (2013). High‐molecular‐mass hyaluronan mediates the cancer resistance of the naked mole rat. Nature, 499(7458), 346–349. https://doi.org/10.1038/nature12234
Tollis, M., Robbins, J., Webb, A. E., Kuderna, L. F. K., Caulin, A. F., Garcia, J. D., Bèrubè, M., Pourmand, N., Marques‐Bonet, T., O'Connell, M. J., Palsbøll, P. J., Maley, C. C., & Shapiro, B. (2019). Return to the sea, get huge, beat cancer: An analysis of cetacean genomes including an assembly for the humpback whale (Megaptera novaeangliae). Molecular Biology and Evolution, 36(8), 1746–1763. https://doi.org/10.1093/molbev/msz099
Tollis, M., Schiffman, J. D., & Boddy, A. M. (2017). Evolution of cancer suppression as revealed by mammalian comparative genomics. Current Opinion in Genetics and Development, 42, 40–47. https://doi.org/10.1016/j.gde.2016.12.004
Tollis, M., Schneider‐Utaka, A. K., & Maley, C. C. (2020). The evolution of human cancer gene duplications across mammals. Molecular Biology and Evolution, 37(10), 2875–2886. https://doi.org/10.1101/2020.03.05.978965
Turbill, C., Bieber, C., & Ruf, T. (2011). Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proceedings of the Royal Society B: Biological Sciences, 278(1723), 3355–3363. https://doi.org/10.1098/rspb.2011.0190
Ujvari, B., & Belov, K. (2011). Major histocompatibility complex (MHC) markers in conservation biology. International Journal of Molecular Sciences, 12(8), 5168–5186. https://doi.org/10.3390/ijms12085168
Ujvari, B., Gatenby, R. A., & Thomas, F. (2016a). The evolutionary ecology of transmissible cancers. Infection, Genetics and Evolution, 39, 293–303. https://doi.org/10.1016/j.meegid.2016.02.005
Ujvari, B., Gatenby, R. A., & Thomas, F. (2016b). Transmissible cancers, are they more common than thought? Evolutionary Applications, 9(5), 633–634. https://doi.org/10.1111/eva.12372
Ujvari, B., Klaassen, M., Raven, N., Russell, T., Vittecoq, M., Hamede, R., Thomas, F., & Madsen, T. (2018). Genetic diversity, inbreeding and cancer. Proceedings of the Royal Society B: Biological Sciences, 285(1875), 20172589. https://doi.org/10.1098/rspb.2017.2589
Vincze, O., Colchero, F., Lemaître, J. F., Conde, D. A., Pavard, S., Bieuville, M., Urrutia, A. O., Ujvari, B., Boddy, A. M., Maley, C. C., Thomas, F., & Giraudeau, M. (2022). Cancer risk across mammals. Nature, 601(7892), 263–267. https://doi.org/10.1038/s41586‐021‐04224‐5
Vittecoq, M., Giraudeau, M., Sepp, T., Marcogliese, D. J., Klaassen, M., Renaud, F., Ujvari, B., & Thomas, F. (2018). Turning natural adaptations to oncogenic factors into an ally in the war against cancer. Evolutionary Applications, 11(6), 836–844. https://doi.org/10.1111/eva.12608
Vittecoq, M., Roche, B., Daoust, S. P., Ducasse, H., Missé, D., Abadie, J., Labrut, S., Renaud, F., Gauthier‐Clerc, M., & Thomas, F. (2013). Cancer: A missing link in ecosystem functioning? Trends in Ecology & Evolution, 28(11), 628–635. https://doi.org/10.1016/j.tree.2013.07.005
Wang, X., Chen, S., & Jia, W. (2016). Metabolomics in cancer biomarker research. Current Pharmacology Reports, 2(6), 293–298. https://doi.org/10.1007/s40495‐016‐0074‐x
Werner, M., Chott, A., Fabiano, A., & Battifora, H. (2000). Effect of formalin tissue fixation and processing on immunohistochemistry. The American Journal of Surgical Pathology, 24(7), 1016–1019.
Wilkinson, G. S., & Adams, D. M. (2019). Recurrent evolution of extreme longevity in bats. Biology Letters, 15(4), 20180860. https://doi.org/10.1098/rsbl.2018.0860
Wright, T., Brisson, B. A., Wood, G. A., Oblak, M., Mutsaers, A. J., Sabine, V., Skowronski, K., Belanger, C., Tiessen, A., & Bienzle, D. (2019). Flow cytometric detection of circulating osteosarcoma cells in dogs. Cytometry Part A, 95(9), 997–1007. https://doi.org/10.1002/cyto.a.23847
Wu, R. S. S. (2002). Hypoxia: From molecular responses to ecosystem responses. Marine Pollution Bulletin, 45(1–12), 35–45. https://doi.org/10.1016/S0025‐326X(02)00061‐9
Ylitalo, G. M., Stein, J. E., Hom, T., Johnson, L. L., Tilbury, K. L., Hall, A. J., Rowles, T., Greig, D., Lowenstine, L. J., & Gulland, F. M. D. (2005). The role of organochlorines in cancer‐associated mortality in California sea lions (Zalophus californianus). Marine Pollution Bulletin, 50(1), 30–39. https://doi.org/10.1016/J.MARPOLBUL.2004.08.005
Zhang, G., Cowled, C., Shi, Z., Huang, Z., Bishop‐Lilly, K. A., Fang, X., Wynne, J. W., Xiong, Z., Baker, M. L., Zhao, W., Tachedjian, M., Zhu, Y., Zhou, P., Jiang, X., Ng, J., Yang, L., Wu, L., Xiao, J., Feng, Y., … Wang, J. (2013). Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science, 339(6118), 456–460. https://doi.org/10.1126/science.1230835