Abstract
In this chapter, we explore whether the mismatch between current lifestyle exposures and those of our ancestral, Neolithic environments substantially escalates an intrinsic risk of cancer. We present data that supports the mismatch concept for the common cancers (skin, breast and prostate) of modern or affluent societies as well as for the cancers in less developed societies. We discuss the open questions in this area, focusing on the constraints and trade-offs underlying cancer susceptibility. Then, we note a number of obstacles to making progress in this area and how those might be overcome. We conclude by suggesting several fruitful directions for future research.
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Greaves M (2014) Does everyone develop covert cancer? Nat Rev Cancer 14(4):209–210
Bissell MJ, Hines WC (2011) Why don’t we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 17(3):320–329
American Cancer Society (2015) Cancer facts & figures 2015. American Cancer Society, Atlanta
Nesse RM (2005) Maladaptation and natural selection. Q Rev Biol 80(1):62–70
Williams GC, Nesse RM (1991) The dawn of darwinian medicine. Q Rev Biol 66(1):1–22
Stearns SC (2012) Evolutionary medicine: its scope, interest and potential. Proc R Soc B Biol Sci 279(1746):4305–4321
Eaton SB, Konner M, Shostak M (1988) Stone agers in the fast lane: chronic degenerative diseases in evolutionary perspective. Am J Med 84(4):739–749
Greaves M (2007) Darwinian medicine: a case for cancer. Nat Rev Cancer 7(3):213–221
Greaves MF (2000) Cancer: the evolutionary legacy. Oxford University Press, Oxford
Irons W (1998) Adaptively relevant environments versus the environment of evolutionary adaptedness. Evol Anthropol 6(6):194–204
Jablonski NG, Chaplin G (2010) Colloquium paper: human skin pigmentation as an adaptation to UV radiation. Proc Natl Acad Sci U S A 107(Suppl 2):8962–8968
Coe K, Steadman L (1995) The human breast and the ancestral reproductive cycle. Hum Nat 6(3):197–220
Strassmann BI (1999) Menstrual cycling and breast cancer: an evolutionary perspective. J Womens Health 8(2):193–202
Eaton SB et al (1994) Women’s reproductive cancers in evolutionary context. Q Rev Biol 69(3):353–367
Wolin KY, Carson K, Colditz GA (2010) Obesity and cancer. Oncologist 15(6):556–565
Sauer LA et al (2005) Eicosapentaenoic acid suppresses cell proliferation in MCF-7 human breast cancer xenografts in nude rats via a pertussis toxin-sensitive signal transduction pathway. J Nutr 135(9):2124–2129
Goh KL (2007) Changing trends in gastrointestinal disease in the Asia–Pacific region. J Dig Dis 8(4):179–185
Krieger N et al (2003) Breast cancer, birth cohorts, and Epstein-Barr virus: methodological issues in exploring the “hygiene hypothesis” in relation to breast cancer, Hodgkin’s disease, and stomach cancer. Cancer Epidemiol Biomarkers Prev 12(5):405–411
Davis CD, Milner JA (2009) Gastrointestinal microflora, food components and colon cancer prevention. J Nutr Biochem 20(10):743–752
Peto R et al (2000) Smoking, smoking cessation, and lung cancer in the UK since 1950: combination of national statistics with two case-control studies. BMJ 321(7257):323–329
Henderson DW et al (2004) After Helsinki: a multidisciplinary review of the relationship between asbestos exposure and lung cancer, with emphasis on studies published during 1997–2004. Pathology 36(6):517–550
Moysich KB, Menezes RJ, Michalek AM (2002) Chernobyl-related ionising radiation exposure and cancer risk: an epidemiological review. Lancet Oncol 3(5):269–279
Birnbaum LS, Fenton SE (2003) Cancer and developmental exposure to endocrine disruptors. Environ Health Perspect 111(4):389
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (1992) Solar and ultraviolet radiation. IARC monographs on carcinogenic risks to humans, vol 55
Greaves M (2014) Was skin cancer a selective force for black pigmentation in early hominin evolution? Proc R Soc B Biol Sci 281(1781):20132955
Scherer D, Kumar R (2010) Genetics of pigmentation in skin cancer - a review. Mutat Res 705(2):141–153
Harding RM et al (2000) Evidence for variable selective pressures at MC1R. Am J Hum Genet 66(4):1351–1361
Jablonski NG, Chaplin G (2010) Human skin pigmentation as an adaptation to UV radiation. Proc Natl Acad Sci U S A 107:8962–8968
Loomis WF (1967) Skin-pigment regulation of vitamin-D biosynthesis in man. Science 157(3788):501–506
Houghton AN, Polsky D (2002) Focus on melanoma. Cancer Cell 2(4):275–278
Byrne C et al (1995) Mammographic features and breast-cancer risk - effects with time, age, and menopause status. J Natl Cancer Inst 87(21):1622–1629
Hulka BS, Stark AT (1995) Breast-cancer - cause and prevention. Lancet 346(8979):883–887
Lipworth L (1995) Epidemiology of breast-cancer. Eur J Cancer Prev 4(1):7–30
Pike MC et al (1983) Hormonal risk-factors, breast-tissue Age and the age-incidence of breast-cancer. Nature 303(5920):767–770
Johnson PA, Giles JR (2013) The hen as a model of ovarian cancer. Nat Rev Cancer 13(6):432–436
Narod SA (2011) Hormone replacement therapy and the risk of breast cancer. Nat Rev Clin Oncol 8(11):669–676
Symmers WSC (1968) Carcinoma of breast in trans-sexual individuals after surgical and hormonal interference with primary and secondary sex characteristics. Br Med J 2(5597):83–85
Marlowe FW (2005) Hunter-gatherers and human evolution. Evol Anthropol 14(2):54–67
Martin JA et al (2015) Births: final data for 2013. Natl Vital Stat Rep 64(1):1–65, National Center for Health Statistics
Centers for Disease Control and Prevention (2014) Breastfeeding report card—United States, 2014
Aktipis CA et al (2014) Modern reproductive patterns associated with estrogen receptor positive but not negative breast cancer susceptibility. Evol Med Public Health 2015(1):52–74
Welch HG, Black WC (1997) Using autopsy series to estimate the disease “reservoir” for ductal carcinoma in situ of the breast: how much more breast cancer can we find? Ann Intern Med 127(11):1023–1028
Sakr WA et al (1993) The frequency of carcinoma and intraepithelial neoplasia of the prostate in young male-patients. J Urol 150(2):379–385
Coffey DS (2001) Similarities of prostate and breast cancer: evolution, diet, and estrogens. Urology 57(4A):31–38
Lichtenstein P et al (2000) Environmental and heritable factors in the causation of cancer - analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 343(2):78–85
Gronberg H (2003) Prostate cancer epidemiology. Lancet 361(9360):859–864
Greaves M (2002) Cancer causation: the Darwinian downside of past success? Lancet Oncol 3(4):244–251
Szabo CI, King MC (1997) Population genetics of BRCA1 and BRCA2. Am J Hum Genet 60(5):1013–1020
Smith KR et al (2011) Effects of BRCA1 and BRCA2 mutations on female fertility. Proceedings. Biological sciences/The Royal Society
Irvine RA et al (1995) The Cag and Ggc microsatellites of the androgen receptor gene are in linkage disequilibrium in men with prostate-cancer. Cancer Res 55(9):1937–1940
Eeles RA et al (2008) Multiple newly identified loci associated with prostate cancer susceptibility. Nat Genet 40(3):316–321
Garcia-Closas M et al (2013) Genome-wide association studies identify four ER negative-specific breast cancer risk loci. Nat Genet 45(4):392–398
Dunbier AK et al (2011) ESR1 is co-expressed with closely adjacent uncharacterised genes spanning a breast cancer susceptibility locus at 6q25.1. PLoS Genet 7(4):e1001382
Ghoussaini M et al (2012) Genome-wide association analysis identifies three new breast cancer susceptibility loci. Nat Genet 44(3):312–318
Low YL et al (2010) Multi-variant pathway association analysis reveals the importance of genetic determinants of estrogen metabolism in breast and endometrial cancer susceptibility. PLoS Genet 6(7):e1001012
Johnson N et al (2012) CYP3A variation, premenopausal estrone levels, and breast cancer risk. J Natl Cancer Inst 104(9):657–669
Prescott J et al (2012) Genome-wide association study of circulating estradiol, testosterone, and sex hormone-binding globulin in postmenopausal women. PLoS One 7(6), e37815
Scheinfeldt LB, Tishkoff SA (2013) Recent human adaptation: genomic approaches, interpretation and insights. Nat Rev Genet 14(10):692–702
Kamberov YG et al (2013) Modeling recent human evolution in mice by expression of a selected EDAR variant. Cell 152(4):691–702
Harris EE, Meyer D (2006) The molecular signature of selection underlying human adaptations. Am J Phys Anthropol 131(S43):89–130
Voight BF et al (2006) A map of recent positive selection in the human genome. PLoS Biol 4(3), e72
Nielsen R et al (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3(6), e170
Sabeti PC et al (2007) Genome-wide detection and characterization of positive selection in human populations. Nature 449(7164):913–918
Rapley EA et al (2009) A genome-wide association study of testicular germ cell tumor. Nat Genet 41(7):807–810
Moutsianas L et al (2011) Multiple Hodgkin lymphoma–associated loci within the HLA region at chromosome 6p21. 3. Blood 118(3):670–674
Zur Hausen H (2007) Infections causing human cancer. Wiley, Hoboken
Goedert JJ (2000) Infectious causes of cancer: targets for intervention. Springer, New York
Ewald PW, Ewald HAS (2012) Infection, mutation, and cancer evolution. J Mol Med 90(5):535–541
Arthur JC et al (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338(6103):120–123
Hill AVS (2001) The genomics and genetics of human infectious disease susceptibility. Annu Rev Genomics Hum Genet 2:373–400
Schetter AJ, Heegaard NH, Harris CC (2010) Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis 31(1):37–49
Culley FJ, Pollott J, Openshaw PJ (2002) Age at first viral infection determines the pattern of T cell–mediated disease during reinfection in adulthood. J Exp Med 196(10):1381–1386
Harker JA et al (2010) Delivery of cytokines by recombinant virus in early life alters the immune response to adult lung infection. J Virol 84(10):5294–5302
Rook GA (2009) The hygiene hypothesis and Darwinian medicine. Springer, New York
Cozen W et al (2009) A protective role for early oral exposures in the etiology of young adult Hodgkin lymphoma. Blood 114(19):4014–4020
Greaves M (2006) Infection, immune responses and the aetiology of childhood leukaemia. Nat Rev Cancer 6(3):193–203
Greaves M (2009) The ‘delayed infection’(aka ‘hygiene’) hypothesis for childhood leukaemia. In: Rook GA (ed) The hygiene hypothesis and Darwinian medicine. Springer, Basel, pp 239–255
Spix C et al (2008) Temporal trends in the incidence rate of childhood cancer in Germany 1987–2004. Int J Cancer 122(8):1859–1867
Surtees PG et al (2010) No evidence that social stress is associated with breast cancer incidence. Breast Cancer Res Treat 120(1):169–174
Keinan-Boker L et al (2009) Cancer incidence in Israeli Jewish survivors of World War II. J Natl Cancer Inst 101(21):1489–1500
Elias SG et al (2004) Breast cancer risk after caloric restriction during the 1944-1945 Dutch famine. J Natl Cancer Inst 96(7):539–546
Koupil I et al (2009) Cancer mortality in women and men who survived the siege of Leningrad (1941-1944). Int J Cancer 124(6):1416–1421
Jacobs JR, Bovasso GB (2000) Early and chronic stress and their relation to breast cancer. Psychol Med 30(3):669–678
Eskelinen M, Ollonen P (2010) Life stress due to losses and deficit in childhood and adolescence as breast cancer risk factor: a prospective case-control study in Kuopio, Finland. Anticancer Res 30(10):4303–4308
Williams JB et al (2009) A model of gene-environment interaction reveals altered mammary gland gene expression and increased tumor growth following social isolation. Cancer Prev Res (Phila) 2(10):850–861
Hermes GL, McClintock MK (2008) Isolation and the timing of mammary gland development, gonadarche, and ovarian senescence: implications for mammary tumor burden. Dev Psychobiol 50(4):353–360
Schwarz S, Messerschmidt H, Dören M (2007) Psychosocial risk factors for cancer development. Med Klin (Munich) 102(12):967–979
Reiche EMV, Nunes SOV, Morimoto HK (2004) Stress, depression, the immune system, and cancer. Lancet Oncol 5(10):617–625
Archer J (2006) Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci Biobehav Rev 30(3):319–345
Alvarado LC (2013) Do evolutionary life-history trade-offs influence prostate cancer risk? a review of population variation in testosterone levels and prostate cancer disparities. Evol Appl 6(1):117–133
Stanton SJ, Schultheiss OC (2007) Basal and dynamic relationships between implicit power motivation and estradiol in women. Horm Behav 52(5):571–580
Boddy AM et al (2015) Cancer susceptibility and reproductive trade-offs: a model of the evolution of cancer defences. Philos Trans R Soc Lond B Biol Sci 370(1673):20140220
Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449(7164):811–818
Arthur JC, Jobin C (2011) The struggle within: microbial influences on colorectal cancer. Inflamm Bowel Dis 17(1):396–409
Elinav E et al (2013) Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer 13(11):759–771
Aktipis C, Nesse RM (2013) Evolutionary foundations for cancer biology. Evol Appl 6(1):144–159
Pédron T et al (2012) A crypt-specific core microbiota resides in the mouse colon. MBio 3(3):e00116-12
Fakhry S et al (2009) Characterization of intestinal bacteria tightly bound to the human ileal epithelium. Res Microbiol 160(10):817–823
Cherbuy C et al (2010) Microbiota matures colonic epithelium through a coordinated induction of cell cycle-related proteins in gnotobiotic rat. Am J Physiol Gastrointest Liver Physiol 299(2):G348–G357
Ulrich CM, Steindorf K, Berger NA (2013) Exercise, energy balance and cancer. Springer, New York
Hsu PP, Sabatini DM (2008) Cancer cell metabolism: warburg and beyond. Cell 134(5):703–707
Weinhouse S et al (1956) On respiratory impairment in cancer cells., http://adsabs.harvard.edu/abs/1956Sci…124.267W
Cairns RA, Harris IS, Mak TW (2011) Regulation of cancer cell metabolism. Nat Rev Cancer 11(2):85–95
Greenwald P, Clifford CK, Milner JA (2001) Diet and cancer prevention. Eur J Cancer 37(8):948–965
Gatenby RA, Gawlinski ET (2003) The glycolytic phenotype in carcinogenesis and tumor invasion: insights through mathematical models. Cancer Res 63(14):3847–3854
Robinson GE, Fernald RD, Clayton DF (2008) Genes and social behavior. Science 322(5903):896–900
Weaver ICG et al (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7(8):847–854
Silverman MN, Sternberg EM (2012) Glucocorticoid regulation of inflammation and its functional correlates: from HPA axis to glucocorticoid receptor dysfunction. Ann N Y Acad Sci 1261:55–63
Volden PA et al (2013) Chronic social isolation is associated with metabolic gene expression changes specific to mammary adipose tissue. Cancer Prev Res (Phila) 6(7):634–645
Champagne FA (2010) Epigenetic influence of social experiences across the lifespan. Dev Psychobiol 52(4):299–311
Roth TL, Sweatt JD (2011) Epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development. J Child Psychol Psychiatry 52(4):398–408
Hidaka BH et al (2015) The status of evolutionary medicine education in North American medical schools. BMC Med Educ 15(1):38
Nesse RM et al (2010) Making evolutionary biology a basic science for medicine. Proc Natl Acad Sci 107(Suppl 1):1800–1807
Acknowledgements
This work has been partially supported by the Sir John Templeton Foundation, National Institutes of Health (R01 CA170595), the Department of Psychology at Arizona State University, the Center for Evolution and Cancer at UCSF and the Centre for Evolution and Cancer at the Institute of Cancer Research, London.
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Greaves, M., Aktipis, C.A. (2016). Mismatches with Our Ancestral Environments and Cancer Risk. In: Maley, C., Greaves, M. (eds) Frontiers in Cancer Research. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-6460-4_10
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