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The evolution of resistance and tolerance as cancer defences

Published online by Cambridge University Press:  11 December 2019

Frédéric Thomas Open the ORCID record for Frédéric Thomas [Opens in a new window] ,
Mathieu Giraudeau ,
Flora Gouzerh ,
Justine Boutry ,
François Renaud ,
Pascal Pujol ,
Aurélie Tasiemski ,
Florence Bernex ,
Antonio Maraver  and
Emilie Bousquet
...Show all authors
Frédéric Thomas*
Affiliation:
CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France
Mathieu Giraudeau
Affiliation:
CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France
Flora Gouzerh
Affiliation:
CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France
Justine Boutry
Affiliation:
CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France
François Renaud
Affiliation:
CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France
Pascal Pujol
Affiliation:
CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France Service de Génétique Médicale et Chromosomique. Unité d'Oncogénétique, CHRU de Montpellier, Hôpital Arnaud de Villeneuve, 371 Avenue du Doyen Gaston Giraud, 34295Montpellier, France
Aurélie Tasiemski
Affiliation:
SPICI, Université de Lille, France
Florence Bernex
Affiliation:
IRCM/RHEM, ICM, BioCampus Montpellier, CNRS, INSERM, Univ Montpellier, Montpellier, France
Antonio Maraver
Affiliation:
IRCM/RHEM, ICM, BioCampus Montpellier, CNRS, INSERM, Univ Montpellier, Montpellier, France
Emilie Bousquet
Affiliation:
IRCM/RHEM, ICM, BioCampus Montpellier, CNRS, INSERM, Univ Montpellier, Montpellier, France
Laurent Dormont
Affiliation:
Centre d'Ecologie Fonctionnelle et Evolutive, CNRS UMR 5175, Montpellier Cedex 5, France
Jens Osterkamp
Affiliation:
Department of Surgery and Transplantation, Rigshospitalet, Blegdamsvej, DK -2100Copenhagen Ø, Denmark
Benjamin Roche
Affiliation:
CREEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France IRD, Sorbonne Université, UMMISCO, F-93143, Bondy, France Departamento de Etología, Fauna Silvestre y Animales de Laboratorio, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México (UNAM), Ciudad de México, México
Rodrigo Hamede
Affiliation:
School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tasmania, 7001, Australia Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Waurn Ponds, Victoria, 3216, Australia
Beata Ujvari
Affiliation:
School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tasmania, 7001, Australia Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Waurn Ponds, Victoria, 3216, Australia
*
Author for correspondence: Frédéric Thomas, E-mail: frederic.thomas2@ird.fr
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Abstract

Although there is a plethora of cancer associated-factors that can ultimately culminate in death (cachexia, organ impairment, metastases, opportunistic infections, etc.), the focal element of every terminal malignancy is the failure of our natural defences to control unlimited cell proliferation. The reasons why our defences apparently lack efficiency is a complex question, potentially indicating that, under Darwinian terms, solutions other than preventing cancer progression are also important contributors. In analogy with host-parasite systems, we propose to call this latter option ‘tolerance’ to cancer. Here, we argue that the ubiquity of oncogenic processes among metazoans is at least partially attributable to both the limitations of resistance mechanisms and to the evolution of tolerance to cancer. Deciphering the ecological contexts of alternative responses to the cancer burden is not a semantic question, but rather a focal point in understanding the evolutionary ecology of host-tumour relationships, the evolution of our defences, as well as why and when certain cancers are likely to be detrimental for survival.

Keywords

CancerResistanceTolerance
Type
Review Article
Information
Parasitology , Volume 147 , Issue 3 , March 2020 , pp. 255 - 262
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Copyright
Copyright © Cambridge University Press 2019

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References

Abegglen, LM, Caulin, AF, Chan, A, Lee, K, Robinson, R, Campbell, MS, Kiso, WK, Schmitt, DL, Waddell, PJ, Bhaskara, S, Jensen, ST, Maley, CC and Schiffman, JD (2015) Potential mechanisms for cancer resistance in elephants and comparative cellular response to DNA damage in humans. JAMA 314, 1850–1860.CrossRefGoogle ScholarPubMed
Adamo, SA (1999) Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Animal Behaviour 57, 117–124.CrossRefGoogle ScholarPubMed
Arnal, A, Tissot, T, Ujvari, B, Nunney, L, Solary, E, Laplane, L, Bonhomme, F, Vittecoq, M, Tasiemski, A and Renaud, F (2016) The guardians of inherited oncogenic vulnerabilities. Evolution 70, 1–6.CrossRefGoogle ScholarPubMed
Arnal, A, Jacqueline, C, Ujvari, B, Leger, L, Moreno, C, Faugere, D, Tasiemski, A, Boidin-Wichlacz, C, Misse, D and Renaud, F (2017) Cancer brings forward oviposition in the fly Drosophila melanogaster. Ecology and Evolution 7, 272–276.CrossRefGoogle ScholarPubMed
Becker, JC, Andersen, MH, Schrama, D and Straten, PT (2013) Immune-suppressive properties of the tumor microenvironment. Cancer Immunology Immunotherapy 62, 1137–1148.CrossRefGoogle ScholarPubMed
Best, A, White, A and Boots, M (2008) Maintenance of host variation in tolerance to pathogens and parasites. Proceedings of the National Academy of Sciences 105, 20786.CrossRefGoogle ScholarPubMed
Carval, D and Ferriere, R (2010) A unified model for the coevolution of resistance, tolerance, and virulence. Evolution 64, 2988–3009.Google ScholarPubMed
Caulin, AF and Maley, CC (2011). Peto's Paradox: evolution's prescription for cancer prevention. Trends in Ecology and Evolution 26, 175–182.CrossRefGoogle Scholar
Crespi, B. and Summers, K (2005) Evolutionary biology of cancer. Trends in Ecology and Evolution 20, 545–552.CrossRefGoogle ScholarPubMed
Das, U and Das, A (2000) Review of canine transmissible venereal sarcoma. Veterinary Research Communications 24, 545–556.CrossRefGoogle ScholarPubMed
d'Avella, D, Salpietro, FM, Alafaci, C and Tomasello, F (1999) Giant olfactory meningiomas: the pterional approach and its relevance for minimizing surgical morbidity. Skull Base Surgery 9, 23–31.CrossRefGoogle ScholarPubMed
Decker, B, Davis, BW, Rimbault, M, Long, AH, Karlins, E, Jagannathan, V, Reiman, R, Parker, HG, Drögemüller, C, Corneveaux, JJ, Chapman, ES, Trent, JM, Leeb, T, Huentelman, MJ, Wayne, RK, Karyadi, DM and Ostrander, EA (2015) Comparison against 186 canid whole-genome sequences reveals survival strategies of an ancient clonally transmissible canine tumor. Genome Research 25, 1646–1655.CrossRefGoogle ScholarPubMed
DeGregori, J (2011) Evolved tumor suppression: why are we so good at not getting cancer? Cancer Research 71, 3739–3744.CrossRefGoogle Scholar
de Lafaille, MAC and Lafaille, JJ (2009) Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30, 626–635.CrossRefGoogle Scholar
Dillman, AR and Schneider, DS (2015) Defining resistance and tolerance to cancer. Cell Reports 13, 884–887.CrossRefGoogle Scholar
Dunn, GP, Old, LJ and Schreiber, RD (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21, 137–148.CrossRefGoogle ScholarPubMed
Easton, DF, Ford, D and Bishop, DT (1995) Breast and ovarian cancer incidence in BRCA1-mutation carriers. Breast Cancer Linkage Consortium. American Journal of Human Genetics 56, 265.Google ScholarPubMed
Engelhardt, SC, Bergeron, P, Gagnon, A, Dillon, L and Pelletier, F (2019) Using geographic distance as a potential proxy for help in the assessment of the grandmother hypothesis. Current Biology 29, 651–656.e653.CrossRefGoogle ScholarPubMed
Epstein, BM, Jones, M, Hamede, R, Hendricks, S, McCallum, H, Murchison, EP, Schönfeld, B, Wiench, C, Hohenlohe, P and Storfer, A (2016) Rapid evolutionary response to a transmissible cancer in Tasmanian devils. Nature Communications 7, 12684–12684.CrossRefGoogle ScholarPubMed
Finlay, BB and McFadden, G (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124, 767–782.CrossRefGoogle ScholarPubMed
Forbes, MR (1993) Parasitism and host reproductive effort. Oikos 67, 444–450.CrossRefGoogle Scholar
Frampton, D, Schwenzer, H, Marino, G, Butcher, LM, Pollara, G, Kriston-Vizi, J, Venturini, C, Austin, R, de Castro, KF, Ketteler, R, Chain, B, Goldstein, RA, Weiss, RA, Beck, S and Fassati, A (2018) Molecular signatures of regression of the Canine Transmissible Venereal Tumor. Cancer Cell 33, 620–633.e626.CrossRefGoogle ScholarPubMed
Gatenby, RA, Silva, AS, Gillies, RJ and Frieden, BR (2009) Adaptive therapy. Cancer Research 69, 4894.CrossRefGoogle ScholarPubMed
Ghiringhelli, F, Ménard, C, Martin, F and Zitvogel, L (2006) The role of regulatory T cells in the control of natural killer cells: relevance during tumor progression. Immunological Reviews 214, 229–238.CrossRefGoogle ScholarPubMed
Giraudeau, M, Sepp, T, Ujvari, B, Ewald, PW and Thomas, F (2018) Human activities might influence oncogenic processes in wild animal populations. Nature Ecology and Evolution 2, 1065–1070.CrossRefGoogle ScholarPubMed
Giraudeau, M, Sepp, T, Ujvari, B, Renaud, F, Tasiemski, A, Roche, B, Capp, JP and Thomas, F (2019) Differences in mutational processes and intra-tumour heterogeneity between organs: the local selective filter hypothesis. Evolution, Medicine, and Public Health 2019, 139–146.CrossRefGoogle ScholarPubMed
Gonzalez, CM, Griffey, SM, Naydan, DK, Flores, E, Cepeda, R, Cattaneo, G and Madewell, BR (2000) Canine transmissible venereal tumour: a morphological and immunohistochemical study of 11 tumours in growth phase and during regression after chemotherapy. Journal of Comparative Pathology 122, 241–248.CrossRefGoogle ScholarPubMed
Hamede, RK, Bashford, J, McCallum, H and Jones, M (2009) Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease. Ecology Letters 12, 1147–1157.CrossRefGoogle Scholar
Hamede, R, Lachish, S, Belov, K, Woods, G, Kreiss, A, Pearse, AM, Lazenby, B, Jones, M and McCallum, H (2012) Reduced effect of Tasmanian devil facial tumor disease at the disease front. Conservation Biology 26, 124–134.CrossRefGoogle ScholarPubMed
Hamede, RK, McCallum, H and Jones, M (2013) Biting injuries and transmission of Tasmanian devil facial tumour disease. Journal of Animal Ecology 82, 182–190.CrossRefGoogle ScholarPubMed
Hamede, RK, Pearse, AM, Swift, K, Barmuta, LA, Murchison, EP and Jones, ME (2015) Transmissible cancer in Tasmanian devils: localized lineage replacement and host population response. Proceedings of the Royal Society of London B: Biological Sciences 282, 20151468.CrossRefGoogle Scholar
Hart, BL (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neuroscience and Biobehavioral Reviews 14: 273–294.CrossRefGoogle ScholarPubMed
Hasselquist, D and Nilsson, JA (2012) Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Animal Behaviour 83, 1303–1312.CrossRefGoogle Scholar
Hayward, AD, Garnier, R, Watt, KA, Pilkington, JG, Grenfell, BT, Matthews, JB, Pemberton, JM, Nussey, DH and Graham, AL (2014) Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. The American Naturalist 184, S58–S76.CrossRefGoogle ScholarPubMed
Hochberg, ME, Thomas, F, Assenat, E and Hibner, U (2013) Preventive evolutionary medicine of cancers. Evolutionary Applications 6, 134–143.CrossRefGoogle ScholarPubMed
Hubert, JN, Zerjal, T and Hospital, F (2018) Cancer-and behavior-related genes are targeted by selection in the Tasmanian devil (Sarcophilus harrisii). PloS One 13, e0201838.CrossRefGoogle Scholar
Jacqueline, C, Biro, PA, Beckmann, C, Moller, AP, Renaud, F, Sorci, G, Tasiemski, A, Ujvari, B and Thomas, F (2017) Cancer: a disease at the crossroads of trade-offs. Evolutionary Applications 10, 215–225.CrossRefGoogle ScholarPubMed
Janeway, CA, Travers, P and Walport, M (2001) Pathogens have evolved various means of evading or subverting normal host defenses. In Janeway, CAJ, Travers, P and Walport, M (eds), Immunology: The Immune System in Health and Disease. New York, USA: Garland Science, pp. 1–10.Google Scholar
Jones, ME, Cockburn, A, Hamede, R, Hawkins, C, Hesterman, H, Lachish, S, Mann, D, McCallum, H and Pemberton, D (2008) Life-history change in disease-ravaged Tasmanian devil populations. Proceedings of the National Academy of Sciences 105, 10023–10027.CrossRefGoogle ScholarPubMed
Jurić, S, Jančuljak, D, Tomić, S and Štimac, D (2013) Brain tissue adaptability to slow-growing tumors: case report of clivus meningioma. Collegium Antropologicum 37, 1011–1014.Google ScholarPubMed
Kidd, P (2003) Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Alternative Medicine Review 8, 223–246.Google ScholarPubMed
Klasing, KC (2007) Nutrition and the immune system. British Poultry Science 48, 525–537.CrossRefGoogle ScholarPubMed
Knutson, KL and Disis, ML (2005) Tumor antigen-specific T helper cells in cancer immunity and immunotherapy. Cancer Immunol Immunotherapy 54, 721–728.CrossRefGoogle ScholarPubMed
Lippitz, BE 2013. Cytokine patterns in patients with cancer: a systematic review. The Lancet Oncology 14, e218–e228.CrossRefGoogle ScholarPubMed
Lochmiller, RL and Deerenberg, C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98.CrossRefGoogle Scholar
Lough, GI, Kyriazakis, I, Bergmann, S, Lengeling, A and Doeschl-Wilson, A (2015) Health trajectories reveal the dynamic contributions of host genetic resistance and tolerance to infection outcome. Proceedings of the Royal Society of London B: Biological Sciences. 282, 20152151.CrossRefGoogle ScholarPubMed
Madsen, T, Arnal, A, Vittecoq, M, Bernex, F, Abadie, J, Labrut, S, Garcia, D, Faugère, D, Lemberger, K, Beckmann, C, Roche, B, Thomas, F and Ujvari, B (2017) Chapter 2: Cancer prevalence and etiology in wild and captive animals. In Ujvari, B, Roche, B and Thomas, F (eds). Ecology and Evolution of Cancer. London: Academic Press, pp. 11–46.CrossRefGoogle Scholar
Maher, S, Toomey, D, Condron, C and Bouchier-Hayes, D (2002) Activation-induced cell death: the controversial role of Fas and Fas ligand in immune privilege and tumour counterattack. Immunology and Cell Biology 80, 131–137.CrossRefGoogle ScholarPubMed
Maley, CC (2007) Multistage carcinogenesis in Barrett's esophagus. Cancer Letters 245, 22–32.CrossRefGoogle ScholarPubMed
Mapara, MY and Sykes, M (2004) Tolerance and cancer: mechanisms of tumor evasion and strategies for breaking tolerance. Journal of Clinical Oncology 22, 1136–1151.CrossRefGoogle ScholarPubMed
Margres, MJ, Ruiz-Aravena, M, Hamede, R, Jones, ME, Lawrance, MF, Hendricks, SA, Patton, A, Davis, BW, Ostrander, EA and McCallum, H (2018) The genomic basis of tumor regression in Tasmanian devils (Sarcophilus harrisii). Genome Biology and Evolution 10, 3012–3025.Google Scholar
Matheu, A, Maraver, A, Klatt, P, Flores, I, Garcia-Cao, I, Borras, C, Flores, JM, Viña, J, Blasco, MA and Serrano, M (2007) Delayed ageing through damage protection by the Arf/p53 pathway. Nature 448, 375.CrossRefGoogle ScholarPubMed
Matic, M, Lm Jongen, J, Elens, L, Wildt, S, Tibboel, D, Ae Sillevis Smitt, P and Hn van Schaik, R (2017) Advanced cancer pain: the search for genetic factors correlated with interindividual variability in opioid requirement. Pharmacogenomics 18, DOI: 10.2217/pgs-2017-2060.CrossRefGoogle ScholarPubMed
Mazé-Guilmo, E, Loot, G, Páez, DJ, Lefèvre, T and Blanchet, S (2014) Heritable variation in host tolerance and resistance inferred from a wild host-parasite system. Proceedings of the Royal Society of London B: Biological Sciences 281, 20132567–20132567.CrossRefGoogle ScholarPubMed
Meacham, CE and Morrison, SJ (2013) Tumour heterogeneity and cancer cell plasticity. Nature 501, 328.CrossRefGoogle ScholarPubMed
Medzhitov, R, Schneider, DS and Soares, MP (2012) Disease tolerance as a defense strategy. Science 335, 936–941.CrossRefGoogle ScholarPubMed
Mengelbier, LH, Karlsson, J, Lindgren, D, Valind, A, Lilljebjörn, H, Jansson, C, Bexell, D, Braekeveldt, N, Ameur, A and Jonson, T (2015) Intratumoral genome diversity parallels progression and predicts outcome in pediatric cancer. Nature Communications 6, 6125.CrossRefGoogle ScholarPubMed
Minchella, DJ and Loverde, PT (1981) A cost of increased early reproductive effort in the snail Biomphalaria glabrata. The American Naturalist 118, 876–881.CrossRefGoogle Scholar
Mukaratirwa, S and Gruys, E (2003) Canine transmissible venereal tumour: cytogenetic origin, immunophenotype, and immunobiology. A review. Veterinary Quarterly 25, 101–111.CrossRefGoogle ScholarPubMed
Mumoli, N, Pulerà, F, Vitale, J and Camaiti, A (2013) Frontal lobe syndrome caused by a giant meningioma presenting as depression and bipolar disorder. Singapore Medical Journal 54, e158–e159.CrossRefGoogle ScholarPubMed
Murchison, EP, Schulz-Trieglaff, OB, Ning, Z, Alexandrov, LB, Bauer, MJ, Fu, B, Hims, M, Ding, Z, Ivakhno, S and Stewart, C (2012) Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer. Cell 148, 780–791.CrossRefGoogle ScholarPubMed
Murchison, EP, Wedge, DC, Alexandrov, LB, Fu, B, Martincorena, I, Ning, Z, Tubio, JMC, Werner, EI, Allen, J, De Nardi, AB, Donelan, EM, Marino, G, Fassati, A, Campbell, PJ, Yang, F, Burt, A, Weiss, RA and Stratton, MR (2014) Transmissible dog cancer genome reveals the origin and history of an ancient cell lineage. Science 343, 437–440.CrossRefGoogle ScholarPubMed
Murgia, CL, Pritchard, K, Kim, SY, Fassati, A and Weiss, RA (2006) Clonal origin and evolution of a transmissible cancer. Cell 126, 477–487.CrossRefGoogle ScholarPubMed
Nelson, WG, De Marzo, AM and Isaacs, WB (2003) Prostate cancer. New England Journal of Medicine 349, 366–381.CrossRefGoogle ScholarPubMed
Norris, K and Evans, MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behavioral Ecology 11, 19–26.CrossRefGoogle Scholar
Nunney, L (2018) Size matters: height, cell number and a person's risk of cancer. Proceedings of the Royal Society B: Biological Sciences 285, 20181743.CrossRefGoogle Scholar
Obenauf, AC and Massagué, J (2015) Surviving at a distance: organ specific metastasis. Trends in Cancer 1, 76–91.CrossRefGoogle Scholar
Ostrander, EA, Davis, BW and Ostrander, GK (2016) Transmissible tumors: breaking the cancer paradigm. Trends in Genetics 32, 1–15.CrossRefGoogle ScholarPubMed
Pawełczyk, A, Łojek, E, Rabe-Jabłotiska, J, Pawełczyk, T, Godlewski, B and Radek, M (2012) Depression or apathy? A diagnostic trap: a huge right frontal lobe meningioma diagnosed and treated as mild atypical depression episode – a case study. Psychiatria Polska 46, 903–913.Google ScholarPubMed
Polak, M and Starmer, WT (1998) Parasite–induced risk of mortality elevates reproductive effort in male Drosophila. Proceedings of the Royal Society of London B: Biological Sciences 265, 2197–2201.CrossRefGoogle ScholarPubMed
Pribluda, A, Cecile, C and Jackson, EL (2015) Intratumoral heterogeneity: from diversity comes resistance. Clinical Cancer Research 21, 2916–2923.CrossRefGoogle ScholarPubMed
Pye, RJ, Pemberton, D, Tovar, C, Tubio, JMC, Dun, KA, Fox, S, Darby, J, Hayes, D, Knowles, GA, Kreiss, A, Siddle, HVT, Swift, K, Lyons, AB, Murchison, EP and Woods, GM (2016) A second transmissible cancer in Tasmanian devils. Proceedings of the National Academy of Sciences 113: 374.CrossRefGoogle ScholarPubMed
Råberg, L, Sim, D and Read, AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812.CrossRefGoogle ScholarPubMed
Råberg, L, Graham, AL and Read, AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical transactions of the Royal Society of London. Series B, Biological Sciences 364, 37–49.CrossRefGoogle ScholarPubMed
Reyes-Gibby, CC, Shete, S, Rakvåg, T, Bhat, SV, Skorpen, F, Bruera, E, Kaasa, S and Klepstad, P (2007) Exploring joint effects of genes and the clinical efficacy of morphine for cancer pain: OPRM1 and COMT gene. Pain 130, 25–30.CrossRefGoogle ScholarPubMed
Roerink, SF, Sasaki, N, Lee-Six, H, Young, MD, Alexandrov, LB, Behjati, S, Mitchell, TJ, Grossmann, S, Lightfoot, H and Egan, DA (2018) Intra-tumour diversification in colorectal cancer at the single-cell level. Nature 556, 457.CrossRefGoogle ScholarPubMed
Roy, BA and Kirchner, JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54, 51–63.CrossRefGoogle ScholarPubMed
Ruiz-Aravena, M, Jones, M, Carver, S, Estay, S, Espejo, C, Storfer, A and Hamede, RK (2018) Sex bias in ability to cope with cancer: Tasmanian devils and facial tumour disease. Proceedings of the Royal Society B: Biological Sciences 285, 20182239.CrossRefGoogle ScholarPubMed
Sadd, BM and Schmid-Hempel, P (2009) Principles of ecological immunology. Evolutionary Applications 2, 113–121.CrossRefGoogle ScholarPubMed
Sanchez-Ortiz, RF, Troncoso, P, Babaian, RJ, Lloreta, J, Johnston, DA and Pettaway, CA (2006) African-American men with nonpalpable prostate cancer exhibit greater tumor volume than matched white men. Cancer: Interdisciplinary International Journal of the American Cancer Society 107, 75–82.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P (2011) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford [England]; New York: Oxford University Press.Google Scholar
Sheldon, BC and Verhulst, S (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle ScholarPubMed
Siddle, HV and Kaufman, J (2013) A tale of two tumours: comparison of the immune escape strategies of contagious cancers. Molecular Immunology 55, 190–193.CrossRefGoogle ScholarPubMed
Siddle, HV and Kaufman, J (2015) Immunology of naturally transmissible tumours. Immunology 144, 11–20.CrossRefGoogle ScholarPubMed
Smith, KR, Hanson, HA, Mineau, GP and Buys, SS (2011) Effects of BRCA1 and BRCA2 mutations on female fertility. Proceedings of the Royal Society of London B: Biological Sciences 279, 1389–1395.CrossRefGoogle ScholarPubMed
Sorci, G, Clobert, J and Michalakis, Y (1996) Cost of reproduction and cost of parasitism in the common lizard, Lacerta vivipara. Oikos 76, 121–130.CrossRefGoogle Scholar
Thomas, F, Nesse, R, Gatenby, R, Gidoin, C, Renaud, F and Roche, B (2016) Evolutionary ecology of organs: a missing link in cancer development? Trends in Cancer 2, 409–415.CrossRefGoogle ScholarPubMed
Thomas, F, Jacqueline, C, Tissot, T, Henard, M, Blanchet, S, Loot, G, Dawson, E, Mery, F, Renaud, F, Montagne, J, Beckmann, C, Biro, PA, Hamede, R and Ujvari, B (2017) The importance of cancer cells for animal evolutionary ecology. Nature Ecology and Evolution 1, 1592–1595.CrossRefGoogle ScholarPubMed
Thomas, F, Donnadieu, E, Charriere, GM, Jacqueline, C, Tasiemski, A, Pujol, P, Renaud, F, Roche, B, Hamede, R, Brown, J, Gatenby, R and Ujvari, B (2018 a) Is adaptive therapy natural? PLOS Biology 16, e2007066.CrossRefGoogle ScholarPubMed
Thomas, F, Vavre, F, Tissot, T, Vittecoq, M, Giraudeau, M, Bernex, F, Misse, D, Renaud, F, Raven, N, Beckmann, C, Hamede, R, Biro, PA and Ujvari, B (2018 b) Cancer is not (only) a senescence problem. Trends in Cancer 4, 169–172.CrossRefGoogle Scholar
Tollis, M, Robbins, J, Webb, AE, Kuderna, LFK, Caulin, AF, Garcia, JD, Bèrubè, M, Pourmand, N, Marques-Bonet, T, O'Connell, MJ, Palsbøll, PJ and Maley, CC (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, 1746–1763.CrossRefGoogle Scholar
Tsuzuki, T, Kakegawa, T, Arimori, M, Ueda, M, Watanabe, H, Okamoto, T and Akakura, I (1971) Giant leiomyoma of the esophagus and cardia weighing more than 1000 grams. Chest 60, 396–399.CrossRefGoogle Scholar
Tuna, M, Grocer, AI, Gezercan, Y, Vural, A, Ildan, F, Haciyakupoglu, S and Karadayi, A (1999) Huge meningiomas: a review of 93 cases. Skull Base Surgery 9, 227–238.CrossRefGoogle ScholarPubMed
Ujvari, B, Gatenby, RA and Thomas, F (2016 a) The evolutionary ecology of transmissible cancers. Infection, Genetics and Evolution 39, 293–303.CrossRefGoogle ScholarPubMed
Ujvari, B, Hamede, R, Peck, S, Pemberton, D, Jones, M, Belov, K and Madsen, T (2016 b) Immunoglobulin dynamics and cancer prevalence in Tasmanian devils (Sarcophilus harrisii). Scientific Reports 6, 25093–25093.CrossRefGoogle Scholar
van der Most, PJ, de Jong, B, Parmentier, HK and Verhulst, S (2011) Trade-off between growth and immune function: a meta-analysis of selection experiments. Functional Ecology 25, 74–80.CrossRefGoogle Scholar
van Niekerk, G, Loos, B, Nell, T and Engelbrecht, AM (2016) Cancer tolerance, resistance, pathogenicity and virulence: deconstructing the disease state. Future Oncology 12, 1369–1380.CrossRefGoogle ScholarPubMed
Van Valen, L (1973) A new evolutionary law. Evolutionary Theory 1, 1–30.Google Scholar
Vézilier, J, Nicot, A, Gandon, S and Rivero, A (2015) Plasmodium infection brings forward mosquito oviposition. Biology Letters 11, 20140840.CrossRefGoogle ScholarPubMed
Vittecoq, M, Giraudeau, M, Sepp, T, Marcogliese, DJ, Klaassen, M, Renaud, F, Ujvari, B and Thomas, F (2018) Turning natural adaptations to oncogenic factors into an ally in the war against cancer. Evolutionary Applications 11, 836–844.CrossRefGoogle ScholarPubMed
Wells, K, Hamede, RK, Kerlin, DH, Storfer, A, Hohenlohe, PA, Jones, ME and McCallum, HI (2017) Infection of the fittest: devil facial tumour disease has greatest effect on individuals with highest reproductive output. Ecology Letters 20, 770–778.CrossRefGoogle ScholarPubMed
Wieczorek, G, Asemissen, A, Model, F, Turbachova, I, Floess, S, Liebenberg, V, Baron, U, Stauch, D, Kotsch, K and Pratschke, J (2009) Quantitative DNA methylation analysis of FOXP3 as a new method for counting regulatory T cells in peripheral blood and solid tissue. Cancer Research 69, 599–608.CrossRefGoogle ScholarPubMed
Wright, B, Willet, C, Hamede, R, Jones, M, Belov, K and Wade, C (2017) Variants in the host genome may inhibit tumour growth in devil facial tumours: evidence from genome-wide association. Scientific Reports 7, 1–6.CrossRefGoogle ScholarPubMed
Yang, T. J. 1988. Immunobiology of a spontaneously regressive tumor, the canine transmissible venereal sarcoma (review). Anticancer Research 8, 93–95.Google Scholar
Zhang, W, Edwards, A, Flemington, EK and Zhang, K (2017) Racial disparities in patient survival and tumor mutation burden, and the association between tumor mutation burden and cancer incidence rate. Scientific Reports 7, 13639.CrossRefGoogle ScholarPubMed