Skip to main content
Open Book Publishers

31. Trade-Offs between Mortality Components in Life History Evolution: The Case of Cancers

Chapter of: Human Evolutionary Demography(pp. 715–740)

Export Metadata

  • ONIX 3.0
    • Thoth
    • Project MUSE
      Cannot generate record: No BIC or BISAC subject code
    • OAPEN
    • JSTOR
      Cannot generate record: No BISAC subject code
    • Google Books
      Cannot generate record: No BIC, BISAC or LCC subject code
    • OverDrive
      Cannot generate record: No priced EPUB or PDF URL
  • ONIX 2.1
  • CSV
  • JSON
  • OCLC KBART
  • BibTeX
  • CrossRef DOI deposit
    Cannot generate record: This work does not have any ISBNs
  • MARC 21 Record
    Cannot generate record: MARC records are not available for chapters
  • MARC 21 Markup
    Cannot generate record: MARC records are not available for chapters
  • MARC 21 XML
    Cannot generate record: MARC records are not available for chapters
Metadata
Title31. Trade-Offs between Mortality Components in Life History Evolution
SubtitleThe Case of Cancers
ContributorSamuel Pavard(author)
C. Jessica E. Metcalf(author)
DOIhttps://doi.org/10.11647/obp.0251.31
Landing pagehttps://www.openbookpublishers.com/books/10.11647/obp.0251/chapters/10.11647/obp.0251.31
Licensehttps://creativecommons.org/licenses/by/4.0/
CopyrightS. Pavard; C. J. E. Metcalf;
PublisherOpen Book Publishers
Published on2024-06-14
Long abstractLittle is known about the relative importance of different causes of death in driving the evolution of senescence and longevity across species. Here we argue that cause-specific mortality may be shaped by physiological trade-offs between mortality components, challenging the theoretical view that physiologically independent processes should senesce at the same rate, or that interactions between causes of death will make selection blind to the effects of specific causes of death. We review the evidence that risk of cancers trades off with risks of mortality from other diseases, and investigate whether this might explain two of the most puzzling paradoxes in cancer evolution. First, among species, cancer prevalence is not a function of species’ size and longevity, despite the fact that cancer incidence is known to be a function of the number of cell divisions (and therefore of size) by unit of time (and therefore of longevity). Second, within species, despite the fact that genomic instability is thought to be the proximal cause of both cancer incidence and senescence, mortality rates rise with age while cancer incidence decelerates and declines at old ages. Building on a relatively novel theory from cellular biology, we construct a preliminary model to reveal the degree to which accumulation of senescent cells with age could explain this latter paradox. Diverting damaged stem cells towards a senescent-state reduces their risk of becoming tumorous; however, conversely, the accumulation of senescent cells in tissues compromises their rejuvenation capacity and functioning, leading to organismal senescence. Accumulation of senescent cells with age may then be optimal because it reduces cancer mortality at the cost of faster senescence from other causes. Evolution will drive species towards a balance between these two sources of mortality.
Page rangepp. 715–740
Print length26 pages
LanguageEnglish (Original)
Contributors

Samuel Pavard

(author)
https://orcid.org/0000-0002-6803-8123

Samuel Pavard is Professor at the National Museum of Natural History in Paris. He is a biodemographer with broad interests in understanding the evolution of ageing in humans and across mammals.

C. Jessica E. Metcalf

(author)
https://orcid.org/0000-0003-3166-7521
https://eeb.princeton.edu/people/c-jessica-e-metcalf

C. Jessica E. Metcalf is a Professor at Princeton University, USA. She is a demographer with broad interests in evolutionary ecology, infectious disease dynamics and public policy.

References
  1. L. M. Abegglen, A. F. Caulin, A. Chan, K. Lee, R. Robinson, M. S. Campbell, W. K. Kiso, D. L. Schmitt, P. J. Waddell, S. Bhaskara, S. T. Jensen, C. C. Maley, and J. D. Schiffman. 2015. ‘Potential Mechanisms for Cancer Resistance in Elephants and Comparative Cellular Response to DNA Damage in Humans’, JAMA, 314.17: pp. 1850–60, https://doi.org/10.1001/jama.2015.13134
  2. C. A. Aktipis, A. M. Boddy, G. Jansen, U. Hibner, M. E. Hochberg, C. C. Maley, and G. S. Wilkinson. 2015. ‘Cancer across the Tree of Life: Cooperation and Cheating in Multicellularity’, Philosophical Transactions of the Royal Society B: Biological Sciences, 370.1673, https://doi.org/10.1098/rstb.2014.0219
  3. G. K. Alderton. 2007. ‘Getting Old and Cancer: Hand-in-Hand?’, Nature Reviews Molecular Cell Biology, 8: pp. 676a-76a, https://doi-org.inee.bib.cnrs.fr/10.1038/nrc2215
  4. W. F. Anderson, R. M. Pfeiffer, G. M. Dores, and M. E. Sherman. 2006. ‘Comparison of Age Distribution Patterns for Different Histopathologic Types of Breast Carcinoma’, Cancer Epidemiology Biomarkers & Prevention, 15.10: pp. 1899–905, https://doi.org/10.1158/1055-9965.epi-06-0191
  5. V. N. Anisimov, S. V. Ukraintseva, and A. I. Yashin. 2005. ‘Cancer in Rodents: Does It Tell Us About Cancer in Humans?’, Nat Rev Cancer, 5: pp. 807–19, https://doi.org/10.1038/nrc1715
  6. K. G. Arbeev, S. V. Ukraintseva, L. S. Arbeeva, and A. I. Yashin. 2005. ‘Mathematical Models for Human Cancer Incidence Rates’, Demographic Research, 12: pp. 237-72, https://doi.org/10.4054/demres.2005.12.10
  7. P. Armitage, and R. Doll. 1954. ‘The Age Distribution of Cancer and a Multi-Stage Theory of Carcinogenesis’, Br J Cancer, 8: pp. 1–12, https://doi.org/10.1038/bjc.1954.1
  8. D. J. Baker, B. G. Childs, M. Durik, M. E. Wijers, C. J. Sieben, J. Zhong, R. Saltness, K. B. Jeganathan, G. C. Verzosa, A. Pezeshki, K. Khazaie, J. D. Miller, and J. M. van Deursen. 2016. ‘Naturally Occurring P16ink4a-Positive Cells Shorten Healthy Lifespan’, Nature, 530: pp. 184–89, https://doi.org/10.1038/nature16932
  9. D. J. Baker, T. Wijshake, T. Tchkonia, N. K. LeBrasseur, B. G. Childs, B. van de Sluis, J. L. Kirkland, and J. M. van Deursen. 2011. ‘Clearance of P16ink4a-Positive Senescent Cells Delays Ageing-Associated Disorders’, Nature, 479: pp. 232–36, https://doi.org/10.1038/nature10600
  10. A. Balmain, J. Gray, and B. Ponder. 2003. ‘The Genetics and Genomics of Cancer’, Nat Genet, 33 Suppl: pp. 238–44, https://doi.org/10.1038/ng1107
  11. K. Banno, L. Kisu, M. Yanokura, K. Tsuji, K. Masuda, A. Ueki, Y. Kobayashi, W. Yamagami, H. Nomura, E. Tominaga, N. Susumu, and D. Aoki. 2012. ‘Epimutation and Cancer: A New Carcinogenic Mechanism of Lynch Syndrome’, International journal of oncology, 41.3: pp. 793–97, https://doi.org/10.3892/ijo.2012.1528
  12. A. Bélot, M. Velten, P. Grosclaude, N. Bossard, G. Launoy, L. Remontet, E. Benhamou, L. Chérié-Challine, and others. 2005. ‘Estimation Nationale De L’incidence Et De La Mortalité Par Cancer En France Entre 1980 Et 2005’, Institut de veille sanitaire, p. 132. https://www.santepubliquefrance.fr/docs/estimation-nationale-de-l-incidence-et-de-la-mortalite-par-cancer-en-france-entre-1980-et-2005
  13. R. Buffenstein. 2008. ‘Negligible Senescence in the Longest Living Rodent, the Naked Mole-Rat: Insights from a Successfully Aging Species’, Journal of Comparative Physiology B, 178: pp. 439–45, https://doi.org/10.1007/s00360-007-0237-5
  14. J. Campisi. 2013. ‘Aging, Cellular Senescence, and Cancer’, Annual Review of Physiology, 75: pp. 685–705, 10.1146/annurev-physiol-030212-183653
  15. J. Campisi, and F. d’Adda di Fagagna. 2007. ‘Cellular Senescence: When Bad Things Happen to Good Cells’, Nat Rev Mol Cell Biol, 8: pp. 729–40, https://doi.org/10.1038/nrm2233
  16. M. Casás-Selves, and J. Degregori. 2011. ‘How Cancer Shapes Evolution and How Evolution Shapes Cancer’, Evolution, 4: pp. 624–34, https://doi.org/10.1007/s12052-011-0373-y
  17. S. N. Catlin, L. Busque, R. E. Gale, P. Guttorp, and J. L. Abkowitz. 2011. ‘The Replication Rate of Human Hematopoietic Stem Cells in Vivo’, Blood, 117.17: pp. 4460–66, https://doi.org/10.1182/blood-2010-08-303537
  18. A. F. Caulin, T. A. Graham, L.-S. Wang, and C.C. Maley. 2015. ‘Solutions to Peto’s Paradox Revealed by Mathematical Modelling and Cross-Species Cancer Gene Analysis’, Philosophical Transactions of the Royal Society B: Biological Sciences, 370.1673, https://doi.org/10.1098/rstb.2014.0222
  19. A. F. Caulin, and C. C. Maley. 2011. ‘Peto’s Paradox: Evolution’s Prescription for Cancer Prevention’, Trends Ecol Evol, 26.4: pp. 175–82, https://doi.org/10.1016/j.tree.2011.01.002
  20. W. Chen, R. Zheng, S. Zhang, H. Zeng, Y. Fan, Y. Qiao, and Q. Zhou. 2014. ‘Esophageal Cancer Incidence and Mortality in China, 2010’, Thoracic Cancer, 5.4: pp. 343–48, https://doi.org/10.1111/1759-7714.12100
  21. M. Collado, M. A. Blasco, and M. Serrano. 2007. ‘Cellular Senescence in Cancer and Aging’, Cell, 130.2: pp. 223–33, https://doi.org/10.1016/j.cell.2007.07.003
  22. P. J. Cook, R. Doll, and S. A. Fellingham. 1969. ‘A Mathematical Model for the Age Distribution of Cancer in Man’, Int J Cancer, 4.1: pp. 93–112, https://doi.org/10.1002/ijc.2910040113
  23. L. M. Coussens, and Z. Werb. 2002. ‘Inflammation and Cancer’, Nature, 420: p. 860, https://doi.org/10.1038/nature01322
  24. B. Crespi, and K. Summers. 2005. ‘Evolutionary Biology of Cancer’, Trends in Ecology & Evolution, 20.10: pp. 545–52, https://doi.org/10.1016/j.tree.2005.07.007
  25. C. V. Dang. 2015. ‘A Metabolic Perspective of Peto’s Paradox and Cancer’, Philosophical Transactions of the Royal Society B: Biological Sciences, 370.1673, https://doi.org/10.1098/rstb.2014.0223
  26. J. DeGregori. 2017. ‘Connecting Cancer to Its Causes Requires Incorporation of Effects on Tissue Microenvironments’, Cancer Res, 77.22: pp. 6065–68, https://doi.org/10.1158/0008-5472.CAN-17-1207
  27. —. 2011. ‘Evolved Tumor Suppression: Why Are We So Good at Not Getting Cancer?’, Cancer Res, 71.11: pp. 3739–44, https://doi.org/10.1158/0008-5472.can-11-0342
  28. M. Demaria, M.N. O’Leary, J. Chang, L. Shao, S. Liu, F. Alimirah, K. Koenig, C. Le, N. Mitin, A. M. Deal, S. Alston, E. C. Academia, S. Kilmarx, A. Valdovinos, B. Wang, A. de Bruin, B. K. Kennedy, S. Melov, D. Zhou, N. E. Sharpless, H. Muss, and J. Campisi. 2017. ‘Cellular Senescence Promotes Adverse Effects of Chemotherapy and Cancer Relapse’, Cancer Discov, 7.2: pp. 165–76, https://doi.org/10.1158/2159-8290.cd-16-0241
  29. G. P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, O. Pereira-Smith, and others. 1995. ‘A Biomarker That Identifies Senescent Human Cells in Culture and in Aging Skin in Vivo’, Proc Natl Acad Sci U S A, 92.20: pp. 9363–7, https://doi.org/10.1073/pnas.92.20.9363
  30. L. E. Donate, and M. A. Blasco. 2011. ‘Telomeres in Cancer and Ageing’, Philosophical Transactions of the Royal Society B: Biological Sciences, 366.1561: pp. 76–84, https://doi.org/10.1098/rstb.2010.0291
  31. T. Finkel, M. Serrano, and M. A. Blasco. 2007. ‘The Common Biology of Cancer and Ageing’, Nature, 448: pp. 767–74, https://doi.org/10.1038/nature05985
  32. J. M. Fleming, K. E. Creevy, and D. E. Promislow. 2011. ‘Mortality in North American Dogs from 1984 to 2004: An Investigation into Age-, Size-, and Breed-Related Causes of Death’, J Vet Intern Med, 25.2: pp. 187–98, https://doi.org/10.1111/j.1939-1676.2011.0695.x
  33. J-M. Gaillard, and J-F. Lemaître. 2017. ‘The Williams’ Legacy: A Critical Reappraisal of His Nine Predictions About the Evolution of Senescence’, Evolution, 71.12: pp. 2768–85, https://doi.org/10.1111/evo.13379
  34. V. Gorbunova, A. Seluanov, Z. Zhang, V. N. Gladyshev, and J. Vijg. 2014. ‘Comparative Genetics of Longevity and Cancer: Insights from Long-Lived Rodents’, Nat Rev Genet, 15: pp. 531–40, https://doi.org/10.1038/nrg3728
  35. D. Hanahan, and R. A. Weinberg. 2011. ‘Hallmarks of Cancer: The Next Generation’, Cell, 144.5: pp. 646–74., https://doi.org/10.1016/j.cell.2011.02.013
  36. H. A. Hanson, K. R. Smith, A. M. Stroup, and C. J. Harrell. 2015. ‘An Age-Period-Cohort Analysis of Cancer Incidence among the Oldest Old, Utah 1973–2002’, Population studies, 69.1: pp. 7–22, https://doi.org/10.1080/00324728.2014.958192
  37. C. Harding, F. Pompei, E. E. Lee, and R. Wilson. 2008. ‘Cancer Suppression at Old Age’, Cancer Research, 68.11: pp. 4465–78, https://doi.org/10.1158/0008-5472.can-07-1670
  38. L. Hayflick, and P. S. Moorhead. 1961. ‘The Serial Cultivation of Human Diploid Cell Strains’, Experimental Cell Research, 25.3: pp. 585–621, https://doi.org/10.1016/0014-4827(61)90192-6
  39. A. D. Hayward, J. Moorad, C. E. Regan, C. Berenos, J. G. Pilkington, J. M. Pemberton, and D. H. Nussey. 2015. ‘Asynchrony of Senescence among Phenotypic Traits in a Wild Mammal Population’, Experimental Gerontology, 71: pp. 56–68, https://doi.org/10.1016/j.exger.2015.08.003
  40. C. J. Henry, A. Marusyk, and J. DeGregori. 2011. ‘Aging-Associated Changes in Hematopoiesis and Leukemogenesis: What’s the Connection?’, Aging, 3.6: pp. 643–56, https://doi.org/10.18632/aging.100351
  41. U. Herbig, M. Ferreira, L. Condel, D. Carey, and J. M. Sedivy. 2006. ‘Cellular Senescence in Aging Primates’, Science, 311.5765: p. 1257, https://doi.org/10.1126/science.1122446
  42. M. E. Hochberg, and R. J. Noble. 2017. ‘A Framework for How Environment Contributes to Cancer Risk’, Ecology Letters, 20.2: pp. 117–34, https://doi.org/10.1111/ele.12726
  43. S. Horvath. 2013. ‘DNA Methylation Age of Human Tissues and Cell Types’, Genome Biology, 14: p. 3156, https://doi.org/10.1186/gb-2013-14-10-r115
  44. K. Isler, and C. P. van Schaik. 2006. ‘Metabolic Costs of Brain Size Evolution’, Biology Letters, 2.4: pp. 557–60, https://doi.org/10.1098/rsbl.2006.0538
  45. K. Ito, A. Hirao, F. Arai, S. Matsuoka, K. Takubo, I. Hamaguchi, K. Nomiyama, K. Hosokawa, K. Sakurada, N. Nakagata, Y. Ikeda, T. W. Mak, and T. Suda. 2004. ‘Regulation of Oxidative Stress by ATM Is Required for Self-Renewal of Haematopoietic Stem Cells’, Nature, 431: pp. 997–1002, https://doi.org/10.1038/nature02989
  46. J. C. Jeyapalan, and J. M. Sedivy. 2008. ‘Cellular Senescence and Organismal Aging’, Mechanisms of Ageing and Development, 129.7–8: pp. 467–74, https://doi.org/10.1016/j.mad.2008.04.001
  47. O. R. Jones, A. Scheuerlein, R. Salguero-Gomez, C. G. Camarda, R. Schaible, B. B. Casper, J. P. Dahlgren, J. Ehrlen, M. B. Garcia, E. S. Menges, P. F. Quintana-Ascencio, H. Caswell, A. Baudisch, and J. W. Vaupel. 2014. ‘Diversity of Ageing across the Tree of Life’, Nature, 505: pp. 169–73, https://doi.org/10.1038/nature12789
  48. K.-W. Jung, Y.-J. Won, H.-J. Kong, C.-M. Oh, H. Cho, D.H. Lee, and K.H. Lee. 2015. ‘Cancer Statistics in Korea: Incidence, Mortality, Survival, and Prevalence in 2012’, Cancer Research and Treatment: Official Journal of Korean Cancer Association, 47.2: pp. 127–41, https://doi.org/10.4143/crt.2015.060
  49. W. H. Karasov, and A. E. Douglas. 2013. ‘Comparative Digestive Physiology’, Comprehensive Physiology, 3.2: pp. 741–83, https://doi.org/10.1002/cphy.c110054
  50. T. B. L. Kirkwood. 1977. ‘Evolution of Aging’, Nature, 270: pp. 301–04, https://doi.org/10.1038/270301a0
  51. T. B. L. Kirkwood, and R. Holliday. 1979. ‘The Evolution of Ageing and Longevity’, Proceedings of the Royal Society of London. Series B. Biological Sciences, 205.1161: pp. 531–46, https://doi.org/10.1098/rspb.1979.0083
  52. T. B. L. Kirkwood, and M.R. Rose. 1991. ‘Evolution of Senescence: Late Survival Sacrificed for Reproduction’, Philos Trans R Soc Lond B Biol Sci, 332.1262: pp. 15–24, https://doi.org/10.1098/rstb.1991.0028
  53. A. G. Knudson, Jr. 1971. ‘Mutation and Cancer: Statistical Study of Retinoblastoma’, Proc Natl Acad Sci U S A, 68.4: pp. 820–3, https://doi.org/10.1073/pnas.68.4.820
  54. C. Kraus, S. Pavard, and D. E. Promislow. 2013. ‘The Size-Life Span Trade-Off Decomposed: Why Large Dogs Die Young’, American Naturalist, 181.4: pp. 492–505, https://doi.org/10.1086/669665
  55. T. Kuilman, C. Michaloglou, W. J. Mooi, and D.S. Peeper. 2010. ‘The Essence of Senescence’, Genes Dev, 24: pp. 2463–79, https://doi.org/10.1101/gad.1971610
  56. A. Kulminski, S. V. Ukraintseva, I. Akushevich, K. G. Arbeev, K. Land, and A. I. Yashin. 2007. ‘Accelerated Accumulation of Health Deficits as a Characteristic of Aging’, Experimental Gerontology, 42.10: pp. 963–70, https://doi.org/10.1016/j.exger.2007.05.009
  57. D. Lack. 1947. ‘The Significance of Clutch-Size’, Ibis, 89.2: pp. 302–52, https://doi.org/10.1111/j.1474-919X.1947.tb04155.x
  58. R. Law. 1979. ‘Optimal Life Histories under Age-Specific Predation’, The American Naturalist, 114.3: pp. 399–417. https://doi.org/10.1086/283488
  59. C. Lopez-Otin, M. A. Blasco, L. Partridge, M. Serrano, and G. Kroemer. 2013. ‘The Hallmarks of Aging’, Cell, 153.6: pp. 1194–217, https://doi.org/10.1016/j.cell.2013.05.039
  60. T. Madsen, A. Arnal, M. Vittecoq, F. Bernex, J. Abadie, S. Labrut, D. Garcia, D. Faugere, K. Lemberger, C. Beckman, B. Roche, F. Thomas, and B. Ujvari. 2017. ‘Cancer Prevalence and Etiology in Wild and Captive Animals’, in Ecology and Evolution of Cancer, ed. by B. Ujvari, Roche, B. and Thomas, F (Cambridge, Massachusetts: Academic Press), pp. 10–46, https://doi.org/10.1016/B978-0-12-804310-3.00002-8
  61. T. M. Manini. 2010. ‘Energy Expenditure and Aging’, Ageing Research Reviews, 9.1: pp. 1–11, https://doi.org/10.1016/j.arr.2009.08.002
  62. H. J. Marais, and P. C. Page. 2011. ‘Treatment of Equine Sarcoid in Seven Cape Mountain Zebra (Equus Zebra Zebra)’, Journal of Wildlife Diseases, 47.4: pp. 917–24, https://doi.org/10.7589/0090-3558-47.4.917
  63. M. Massot, J. Clobert, L. Montes-Poloni, C. Haussy, J. Cubo, and S. Meylan. 2011. ‘An Integrative Study of Ageing in a Wild Population of Common Lizards’, Functional Ecology, 25.4: pp. 848–58, https://doi.org/10.1111/j.1365-2435.2011.01837.x
  64. D. McAloose, and A.L. Newton. 2009. ‘Wildlife Cancer: A Conservation Perspective’, Nat Rev Cancer, 9: pp. 517–26, https://doi.org/10.1038/nrc2665
  65. R. Meitern, M.-A. Lind, U. Karu, and P. Hõrak. 2016. ‘Simple and Noninvasive Method for Assessment of Digestive Efficiency: Validation of Fecal Steatocrit in Greenfinch Coccidiosis Model’, Ecology and Evolution, 6.24: pp. 8756–63, https://doi.org/10.1002/ece3.2575
  66. L. Melchor, and J. Benítez. 2013. ‘The Complex Genetic Landscape of Familial Breast Cancer’, Human Genetics, 132: pp. 845–63, https://doi.org/10.1007/s00439-013-1299-y
  67. H. H. Mitchell. 1962. ‘The Maintenance Requirement of Energy: The Basal Metabolim’, in Comparative Nutrition of Man and Domestic Animals (New York and London: Academic Press), pp. 3–90.
  68. A. A. Moskalev, M. V. Shaposhnikov, E. N. Plyusnina, A. Zhavoronkov, A. Budovsky, H. Yanai, and V. E. Fraifeld. 2013. ‘The Role of DNA Damage and Repair in Aging through the Prism of Koch-Like Criteria’, Ageing Research Reviews, 12.2: pp. 661–84, https://doi.org/10.1016/j.arr.2012.02.001
  69. S. C. Nolen, M. A. Evans, A. Fischer, M. M. Corrada, C. H. Kawas, and D. A. Bota. 2017. ‘Cancer-Incidence, Prevalence and Mortality in the Oldest-Old. A Comprehensive Review’, Mech Ageing Dev, 164: pp. 113–26, https://doi.org/10.1016/j.mad.2017.05.002
  70. L. Nunney. 1993. ‘The Influence of Mating System and Overlapping Generations on Effective Population-Size’, Evolution, 47.5: pp. 1329–41, https://doi.org/10.1111/j.1558-5646.1993.tb02158.x
  71. —. 1999. ‘Lineage Selection and the Evolution of Multistage Carcinogenesis’, Proceedings of the Royal Society of London. Series B: Biological Sciences, 266.1418: pp. 493–98, https://doi.org/10.1098/rspb.1999.0664
  72. L. Nunney, and B. Muir. 2015. ‘Peto’s Paradox and the Hallmarks of Cancer: Constructing an Evolutionary Framework for Understanding the Incidence of Cancer’, Philosophical Transactions of the Royal Society B: Biological Sciences, 370.1673, https://doi.org/10.1098/rstb.2015.0161
  73. T. P. O’Connor, A. Lee, J. U. Jarvis, and R. Buffenstein. 2002. ‘Prolonged Longevity in Naked Mole-Rats: Age-Related Changes in Metabolism, Body Composition and Gastrointestinal Function’, Comp Biochem Physiol A Mol Integr Physiol, 133.3: pp. 835–42, https://doi.org/10.1016/S1095-6433(02)00198-8
  74. M. Ogrodnik, S. Miwa, T. Tchkonia, D. Tiniakos, C. L. Wilson, A. Lahat, C. P. Day, A. Burt, A. Palmer, Q. M. Anstee, S. N. Grellscheid, J. H. J. Hoeijmakers, S. Barnhoorn, D. A. Mann, T. G. Bird, W. P. Vermeij, J. L. Kirkland, J. F. Passos, T. von Zglinicki, and D. Jurk. 2017. ‘Cellular Senescence Drives Age-Dependent Hepatic Steatosis’, Nature Communications, 8.1: p. 15691, https://doi.org/10.1038/ncomms15691
  75. R. B. Oriá, P. D. Patrick, J. A. Blackman, A. A. M. Lima, and R. L. Guerrant. 2007. ‘Role of Apolipoprotein E4 in Protecting Children against Early Childhood Diarrhea Outcomes and Implications for Later Development’, Medical hypotheses, 68.5: pp. 1099–107, https://doi.org/10.1016/j.mehy.2006.09.036
  76. S. H. Orzack, and E. Sober. 1994. ‘How (Not) to Test an Optimality Model’, Trends Ecol Evol, 9.7: pp. 265–7, https://doi.org/10.1016/0169-5347(94)90296-8
  77. L. Partridge, R. Sibly, R. J. H. Beverton, and W. G. Hill. 1991. ‘Constraints in the Evolution of Life Histories’, Philosophical Transactions: Biological Sciences, 332.1262: pp. 3–13, https://doi.org/10.1098/rstb.1991.0027
  78. N. Pavlidis, G. Stanta, and R.A. Audisio. 2012. ‘Cancer Prevalence and Mortality in Centenarians: A Systematic Review’, Crit Rev Oncol Hematol, 83.1: pp. 145–52, https://doi.org/10.1016/j.critrevonc.2011.09.007
  79. J. W. Pepper, C. Scott Findlay, R. Kassen, S. L. Spencer, and C. C. Maley. 2009. ‘SYNTHESIS: Cancer Research Meets Evolutionary Biology’, Evolutionary applications, 2.1: pp. 62–70, https://doi.org/10.1111/j.1752-4571.2008.00063.x
  80. R. Peto. 1977. ‘Epidemiology, Multistage Models and Short Term Mutagenicity Tests’, in The Origins of Human Cancer, ed. by H. H. Hiatt, J. D. Watson and J. A. Winsten (Cold Spring Harbor: Cold Spring Harbor Laboratory), pp. 1403–28.
  81. F. Pompei, M. Polkanov, and R. Wilson. 2001. ‘Age Distribution of Cancer in Mice: The Incidence Turnover at Old Age’, Toxicol Ind Health, 17.1: pp. 7–16, https://doi.org/10.1191/0748233701th091oa
  82. H. Pontzer, D. A. Raichlen, A. D. Gordon, K. K. Schroepfer-Walker, B. Hare, M. C. O’Neill, K. M. Muldoon, H. M. Dunsworth, B. M. Wood, K. Isler, J. Burkart, M. Irwin, R. W. Shumaker, E. V. Lonsdorf, and S. R. Ross. 2014. ‘Primate Energy Expenditure and Life History’, Proc Natl Acad Sci U S A, 111.4: pp. 1433–7, https://doi.org/10.1073/pnas.1316940111
  83. A. Rangarajan, and R. A. Weinberg. 2003. ‘Comparative Biology of Mouse Versus Human Cells: Modelling Human Cancer in Mice’, Nat Rev Cancer, 3: pp. 952–59, https://doi.org/10.1038/nrc1235
  84. A. I. Rozhok, and J. DeGregori. 2016. ‘The Evolution of Lifespan and Age-Dependent Cancer Risk’, Trends Cancer, 2.10: pp. 552–60, https://doi.org/10.1016/j.trecan.2016.09.004
  85. P. Schmid-Hempel. 2003. ‘Variation in Immune Defence as a Question of Evolutionary Ecology’, Proceedings of the Royal Society of London. Series B: Biological Sciences, 270.1513: pp. 357–66, https://doi.org/10.1098/rspb.2002.2265
  86. J. W. Shay, and S. Bacchetti. 1997. ‘A Survey of Telomerase Activity in Human Cancer’, European Journal of Cancer, 33: pp. 787–91, https://doi.org/10.1016/S0959-8049(97)00062-2
  87. M. Shpak, and J. Lu. 2016. ‘An Evolutionary Genetic Perspective on Cancer Biology’, Annual Review of Ecology, Evolution, and Systematics, 47: pp. 25–49, https://doi.org/10.1146/annurev-ecolsys-121415-032109
  88. D. W. E. Smith. 1996. ‘Cancer Mortality at Very Old Ages’, Cancer, 77.7: pp. 1367–72, https://doi.org/10.1002/(SICI)1097-0142(19960401)77:7<1367::AID-CNCR22>3.0.CO;2-Z
  89. J. M. Smith. 1962. ‘Review Lectures on Senescence – I. The Causes of Ageing’, Proceedings of the Royal Society of London. Series B. Biological Sciences, 157.966: pp. 115–27, https://doi.org/10.1098/rspb.1962.0065
  90. K. R. Taylor, N. A. Milone, and C. E. Rodriguez. 2017. ‘Four Cases of Spontaneous Neoplasia in the Naked Mole-Rat (Heterocephalus Glaber), a Putative Cancer-Resistant Species’, J Gerontol A Biol Sci Med Sci, 72.1: pp. 38–43, https://doi.org/10.1093/gerona/glw047
  91. C. Tomasetti, L. Li, and B. Vogelstein. 2017. ‘Stem Cell Divisions, Somatic Mutations, Cancer Etiology, and Cancer Prevention’, Science, 355.6331: pp. 1330–34, https://doi.org/10.1126/science.aaf9011
  92. C. Tomasetti, and B. Vogelstein. 2015. ‘Variation in Cancer Risk among Tissues Can Be Explained by the Number of Stem Cell Divisions’, Science, 347.6217: pp. 78–81, https://doi.org/10.1126/science.1260825
  93. J. Tsuchida, M. Nagahashi, O. M. Rashid, K. Takabe, and T. Wakai. 2015. ‘At What Age Should Screening Mammography Be Recommended for Asian Women?’, Cancer Medicine, 4.7: pp. 1136–44, https://doi.org/10.1002/cam4.468
  94. S. V. Ukraintseva, K. G. Arbeev, I. Akushevich, A. Kulminski, L. Arbeeva, I. Culminskaya, L. Akushevich, and A. I. Yashin. 2010. ‘Trade-Offs between Cancer and Other Diseases: Do They Exist and Influence Longevity?’, Rejuvenation Research, 13.4: pp. 387–96, https://doi.org/10.1089/rej.2009.0941
  95. S. V. Ukraintseva, and A. I. Yashin. 2001. ‘How Individual Age-Associated Changes May Influence Human Morbidity and Mortality Patterns’, Mech Ageing Dev, 122.13: pp. 1447–60, https://doi.org/10.1016/s0047-6374(01)00277-9
  96. S.V. Ukraintseva, and A.I. Yashin. 2003. ‘Individual Aging and Cancer Risk: How Are They Related?’, Demographic Research, 9: pp. 163–96, https://doi.org/10.4054/demres.2003.9.8
  97. J. W. Vaupel, K. G. Manton, and E. Stallard. 1979. ‘The Impact of Heterogeneity in Individual Frailty on the Dynamics of Mortality’, Demography, 16.3: pp. 439–54, https://doi.org/10.2307/2061224
  98. J. W. Vaupel, and A. I. Yashin. 1986. ‘Cancer Rates over Age, Time and Place: Insights from Stochastic Models of Heterogeneous Populations’, in IIASA Working Paper.
  99. M. Vittecoq, B. Roche, S. P. Daoust, H. Ducasse, D. Misse, J. Abadie, S. Labrut, F. Renaud, M. Gauthier-Clerc, and F. Thomas. 2013. ‘Cancer: A Missing Link in Ecosystem Functioning?’, Trends Ecol Evol, 28.11: pp. 628–35, https://doi.org/10.1016/j.tree.2013.07.005
  100. B. Vogelstein, N. Papadopoulos, V. E. Velculescu, S. Zhou, L. A. Diaz, and K. W. Kinzler. 2013. ‘Cancer Genome Landscapes’, Science, 339.6127: pp. 1546–58, https://doi.org/10.1126/science.1235122
  101. J. T. Willerson, and P. M. Ridker. 2004. ‘Inflammation as a Cardiovascular Risk Factor’, Circulation, 109: pp. II-2-II-10, https://doi.org/10.1161/01.CIR.0000129535.04194.38
  102. G. C. Williams. 1966. ‘Natural Selection Costs of Reproduction and a Refinement of Lacks Principle’, American Naturalist, 100.916: pp. 687–90, https://doi.org/10.1086/282461
  103. —. 1957. ‘Pleiotropy, Natural-Selection, and the Evolution of Senescence’, Evolution, 11:.4 pp. 398–411, https://doi.org/10.2307/2406060
  104. A. I. Yashin, K. G. Arbeev, A. Kulminski, I. Akushevich, L. Akushevich, and S. V. Ukraintseva. 2007. ‘Health Decline, Aging and Mortality: How Are They Related?’, Biogerontology, 8: pp. 291–302, https://doi.org/10.1007/s10522-006-9073-3
  105. A. I. Yashin, S. V. Ukraintseva, I. V. Akushevich, K. G. Arbeev, A. Kulminski, and L. Akushevich. 2009. ‘Trade-Off between Cancer and Aging: What Role Do Other Diseases Play? Evidence from Experimental and Human Population Studies’, Mechanisms of Ageing and Development, 130.1–2: pp. 98–104, https://doi.org/10.1016/j.mad.2008.03.006
  106. D. R. Youlden, S. M. Cramb, C. H. Yip, and P. D. Baade. 2014. ‘Incidence and Mortality of Female Breast Cancer in the Asia-Pacific Region’, Cancer Biology & Medicine, 11.2: pp. 101–15. https://doi.org/10.7497/j.issn.2095-3941.2014.02.005