Abstract
Somatic evolution during cancer progression and therapy results in tumour cells that show a wide range of phenotypes, which include rapid proliferation and quiescence. Evolutionary life history theory may help us to understand the diversity of these phenotypes. Fast life history organisms reproduce rapidly, whereas those with slow life histories show less fecundity and invest more resources in survival. Life history theory also provides an evolutionary framework for phenotypic plasticity, which has potential implications for understanding 'cancer stem cells'. Life history theory suggests that different therapy dosing schedules might select for fast or slow life history cell phenotypes, with important clinical consequences.
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References
Stearns, S. C. The evolution of life histories (Oxford Univ. Press, 1992).
Stearns, S. C. Trade-offs in life-history evolution. Funct. Ecol. 3, 259–268 (1989).
Williams, G. C. Natural selection, the cost or reproduction and a refinement of Lack's principle. Am. Nat. 100, 687–690 (1966).
Creighton, J. C., Heflin, N. D. & Belk, M. C. Cost of reproduction, resource quality, and terminal investment in a burying beetle. Am. Nat. 174, 673–684 (2009).
Fabian, D. & Flatt, T. Life history evolution. Nature Education Knowledge 3, 24 (2012).
Partridge, L. & Prowse, N. The effects of reproduction on longevity and fertility in male Drosophila melanogaster. J. Insect Physiol. 43, 501–512 (1997).
Zakrzewska, A. et al. Genome-wide analysis of yeast stress survival and tolerance acquisition to analyze the central trade-off between growth rate and cellular robustness. Mol. Biol. Cell 22, 4435–4446 (2011).
Broxterman, H. J. et al. Induction by verapamil of a rapid increase in ATP consumption in multidrug-resistant tumor cells. FASEB J. 2, 2278–2282 (1988).
Vander Heiden, M. G., Cantley, L. C. & Thompson, C. B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029–1033 (2009).
Gatenby, R. A. & Gillies, R. J. Why do cancers have high aerobic glycolysis? Nature Rev. Cancer 4, 891–899 (2004).
Jerby, L. et al. Metabolic associations of reduced proliferation and oxidative stress in advanced breast cancer. Cancer Res. 72, 5712–5720 (2012).
Williams, G. C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (1957).
Leroi, A. M. et al. What evidence is there for the existence of individual genes with antagonistic pleiotropic effects? Mech. Ageing Dev. 126, 421–429 (2005).
Campisi, J. Cellular senescence and apoptosis: how cellular responses might influence aging phenotypes. Exp. Gerontol. 38, 5–11 (2003).
Ungewitter, E. & Scrable, H. Antagonistic pleiotropy and p53. Mech. Ageing Dev. 130, 10–17 (2009).
Jeschke, J. M. & Kokko, H. The roles of body size and phylogeny in fast and slow life histories. Evol. Ecol. 23, 867–878 (2009).
MacArthur, R. & Wilson, E. O. The theory of island biography (Princeton Univ. Press, 1967).
Malthus, T. R. An Essay on the Principle of Population (Johnson, 1798).
Aktipis, C. A., Maley, C. C. & Pepper, J. W. Dispersal evolution in neoplasms: the role of disregulated metabolism in the evolution of cell motility. Cancer Prev. Res. (Phila) 5, 266–275 (2012).
Chen, J., Sprouffske, K., Huang, Q. & Maley, C. C. Solving the puzzle of metastasis: the evolution of cell migration in neoplasms. PLoS ONE 6, e17933 (2011).
Reznick, D. & Bryant, M. J. & Bashey, F. r- and K-selection revisited: The role of population regulation in life-history evolution. Ecology 83, 1509–1520 (2002).
Skutch, A. F. Life history of Longuemare's hermit hummingbird. Int. J. Avain Sci. 93, 180–195 (1951).
Howe, H. F. & Smallwood, J. Ecology of seed dispersal. Ann. Rev. Ecol. Systemat. 13, 201–228 (1982).
Promislow, D. E. L. & Harvey, P. H. Living fast and dying young: A comparative analysis of life-history variation in mammals. J. Zool. 220, 417–437 (1990).
Ebenman, B. Competition between age classes and population dynamics. J. Theor. Biol. 131, 389–400 (1988).
Turnbull, L. A., Rees, M. & Crawley, M. J. Seed mass and the competition/colonization trade-off: a sowing experiment. J. Ecol. 87, 899–912 (1999).
Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57–70 (2000).
Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011).
Gerlinger, M. & Swanton, C. How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine. Br. J. Cancer 103, 1139–1143 (2010).
Gillies, R. J., Verduzco, D. & Gatenby, R. A. Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nature Rev. Cancer 12, 487–493 (2012).
Greaves, M. & Maley, C. C. Clonal evolution in cancer. Nature 481, 306–313 (2012).
Merlo, L. M., Pepper, J. W., Reid, B. J. & Maley, C. C. Cancer as an evolutionary and ecological process. Nature Rev. Cancer 6, 924–935 (2006).
Nowell, P. C. The clonal evolution of tumor cell populations. Science 194, 23–28 (1976).
van Diest, P. J., van der Wall, E. & Baak, J. P. Prognostic value of proliferation in invasive breast cancer: a review. J. Clin. Pathol. 57, 675–681 (2004).
Kreso, A. et al. Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 339, 543–548 (2013).
Orlando, P. A., Gatenby, R. A. & Brown, J. S. Tumor evolution in space: The effects of competition colonization tradeoffs on tumor invasion dynamics. Front. Oncol. http://dx.doi.org/10.3389/fonc.2013.00045 (2013).
Alfarouk, K. O., Ibrahim, M. E., Gatenby, R. A. & Brown, J. S. Riparian ecosystems in human cancers. Evol. Appl. 6, 46–53 (2013).
Brurberg, K. G., Skogmo, H. K., Graff, B. A., Olsen, D. R. & Rofstad, E. K. Fluctuations in pO2 in poorly and well-oxygenated spontaneous canine tumors before and during fractionated radiation therapy. Radiother. Oncol. 77, 220–226 (2005).
Cardenas-Navia, L. I. et al. The pervasive presence of fluctuating oxygenation in tumors. Cancer Res. 68, 5812–5819 (2008).
Limberger, R. & Wickham, S. A. Competition-colonization trade-offs in a ciliate model community. Oecologia 167, 723–732 (2011).
Turchin, P. Does population ecology have general laws? OIKOS 94, 17–26 (2001).
Graham, T. A. et al. Use of methylation patterns to determine expansion of stem cell clones in human colon tissue. Gastroenterology 140, 1241–1250 e1-9 (2011).
Greaves, L. C. et al. Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission. Proc. Natl Acad. Sci. USA 103, 714–719 (2006).
Zhang, W. et al. UVB-induced apoptosis drives clonal expansion during skin tumor development. Carcinogenesis 26, 249–257 (2005).
Cairns, J. Mutation selection and the natural history of cancer. Nature 255, 197–200 (1975).
Kenific, C. M., Thorburn, A. & Debnath, J. Autophagy and metastasis: another double-edged sword. Curr. Opin. Cell Biol. 22, 241–245 (2010).
Debnath, J. & Brugge, J. S. Modelling glandular epithelial cancers in three-dimensional cultures. Nature Rev. Cancer 5, 675–688 (2005).
Etzioni, R. et al. The case for early detection. Nature Rev. Cancer 3, 243–252 (2003).
Seliger, B. Strategies of tumor immune evasion. BioDrugs 19, 347–354 (2005).
Rhim, A. D. et al. EMT and dissemination precede pancreatic tumor formation. Cell 148, 349–361 (2012).
Schmidt-Kittler, O. et al. From latent disseminated cells to overt metastasis: genetic analysis of systemic breast cancer progression. Proc. Natl Acad. Sci. USA 100, 7737–7742 (2003).
Debarre, F. & Gandon, S. Evolution in heterogeneous environments: between soft and hard selection. Am. Nat. 177, E84–E97 (2011).
Wilting, R. H. & Dannenberg, J. H. Epigenetic mechanisms in tumorigenesis, tumor cell heterogeneity and drug resistance. Drug Resist. Updat. 15, 21–38 (2012).
Clevers, H. The cancer stem cell: premises, promises and challenges. Nature Med. 17, 313–319 (2011).
Magee, J. A., Piskounova, E. & Morrison, S. J. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 21, 283–296 (2012).
Holzel, M., Bovier, A. & Tuting, T. Plasticity of tumour and immune cells: a source of heterogeneity and a cause for therapy resistance? Nature Rev. Cancer 13, 365–376 (2013).
Li, L. & Clevers, H. Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542–545 (2010).
Wilson, A. et al. Dormant and self-renewing hematopoietic stem cells and their niches. Ann. NY Acad. Sci. 1106, 64–75 (2007).
Biddle, A. et al. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res. 71, 5317–5326 (2011).
Kusumbe, A. P. & Bapat, S. A. Cancer stem cells and aneuploid populations within developing tumors are the major determinants of tumor dormancy. Cancer Res. 69, 9245–9253 (2009).
Sharma, S. V. et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69–80 (2010).
Godlewski, J. et al. MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol. Cell 37, 620–632 (2010).
West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003).
Houston, A. I. & McNamara, J. M. Phenotypic plasticity as a state-dependent life-history decision. Evol. Ecol. 6, 243–253 (1992).
Gurney, W. S. C. & Middleton, D. A. J. Optimal resource allocation in a randomly varying environment. Funct. Ecol. 10, 602–612 (1996).
Ball, S. L. & Baker, R. L. Predator induced life history changes: Antipredator behavior costs or facultative life history shifts? Ecology 77, 1116–1124 (1996).
Reznick, D., Butler, M. J. & Rodd, H. Life history evolution in guppies. VII. The comparative ecology of high and low predation environments. Am. Nat. 157, 12–26 (2001).
Chivers, D. P., Kiesecker, J. M., Marco, A., Wildy, E. L. & Blaustein, A. R. Shifts in life history as a repsonse to predation in western toads (Bufo boreas). J. Chem. Ecol. 25, 2455–2463 (1999).
Buhse, H. E. Jr & Williams, N. E. A comparison of cortical proteins in Tetrahymena vorax microstomes and macrostomes. J. Protozool. 29, 222–226 (1982).
Ryals, P. E., Smith-Somerville, H. E. & Buhse, H. E. Jr. Phenotype switching in polymorphic Tetrahymena: a single-cell Jekyll and Hyde. Int. Rev. Cytol. 212, 209–238 (2002).
Foret, S. et al. DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc. Natl Acad. Sci. USA 109, 4968–4973 (2012).
Fitzpatrick, M. J. et al. Candidate genes for behavioural ecology. Trends Ecol. Evol. 20, 96–104 (2005).
Smith, C. R., Toth, A. L., Suarez, A. V. & Robinson, G. E. Genetic and genomic analyses of the division of labour in insect societies. Nature Rev. Genet. 9, 735–748 (2008).
O'Brien, C. A., Pollett, A., Gallinger, S. & Dick, J. E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445, 106–110 (2007).
Lapidot, T. et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645–648 (1994).
Gupta, P. B. et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146, 633–644 (2011).
Taussig, D. C. et al. Leukemia-initiating cells from some acute myeloid leukemia patients with mutated nucleophosmin reside in the CD34− fraction. Blood 115, 1976–1984 (2010).
Schlichting, C. D. Origins of differentiation via phenotypic plasticity. Evol. Dev. 5, 98–105 (2003).
Bissell, M. J. & Labarge, M. A. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 7, 17–23 (2005).
Bunt, S. K., Sinha, P., Clements, V. K., Leips, J. & Ostrand-Rosenberg, S. Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 176, 284–290 (2006).
Bunt, S. K. et al. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res. 67, 10019–10026 (2007).
Grivennikov, S. I., Greten, F. R. & Karin, M. Immunity, inflammation, and cancer. Cell 140, 883–899 (2010).
Joyce, J. A. & Pollard, J. W. Microenvironmental regulation of metastasis. Nature Rev. Cancer 9, 239–252 (2009).
Mantovani, A., Allavena, P., Sica, A. & Balkwill, F. Cancer-related inflammation. Nature 454, 436–444 (2008).
Sprouffske, K. et al. An evolutionary explanation for the presence of cancer nonstem cells in neoplasms. Evol. Appl. 6, 92–101 (2013).
Kirkwood, T. B. Evolution of ageing. Mech. Ageing Dev. 123, 737–745 (2002).
Borst, P. Cancer drug pan-resistance: pumps, cancer stem cells, quiescence, epithelial to mesenchymal transition, blocked cell death pathways, persisters or what? Open Biol. 2, 120066 (2012).
Gottesman, M. M., Fojo, T. & Bates, S. E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nature Rev. Cancer 2, 48–58 (2002).
Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nature Rev. Microbiol. 8, 15–25 (2010).
Smith, V. H. & Holt, R. D. Resource competition and within-host disease dynamics. Trends Ecol. Evol. 11, 386–389 (1996).
Wargo, A. R., Huijben, S., de Roode, J. C., Shepherd, J. & Read, A. F. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc. Natl Acad. Sci. USA 104, 19914–19919 (2007).
Gatenby, R. A., Silva, A. S., Gillies, R. J. & Frieden, B. R. Adaptive therapy. Cancer Res. 69, 4894–4903 (2009).
Contractor, K. B. & Aboagye, E. O. Monitoring predominantly cytostatic treatment response with 18F-FDG PET. J. Nucl. Med. 50 (Suppl. 1), 97–105 (2009).
Coffey, J. C. et al. Excisional surgery for cancer cure: therapy at a cost. Lancet Oncol. 4, 760–768 (2003).
Mazzone, M. et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136, 839–851 (2009).
Robey, I. F. et al. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res. 69, 2260–2268 (2009).
Pasquier, E., Kavallaris, M. & Andre, N. Metronomic chemotherapy: new rationale for new directions. Nature Rev. Clin. Oncol. 7, 455–465 (2010).
Crook, J. M. et al. Intermittent androgen suppression for rising PSA level after radiotherapy. N. Engl. J. Med. 367, 895–903 (2012).
Aguirre-Ghiso, J. A. Models, mechanisms and clinical evidence for cancer dormancy. Nature Rev. Cancer 7, 834–846 (2007).
Radich, J. P. & Wood, B. L. in Leukemia and Related Disorders (eds Estey, E. H. & Appelbaum, F. R.) 251–271 (Springer, 2012).
Lu, Z. et al. The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J. Clin. Invest. 118, 3917–3929 (2008).
Wilkinson, G. S. & South, J. M. Life history, ecology and longevity in bats. Aging Cell 1, 124–131 (2002).
Rothwell, P. M. et al. Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials. Lancet 377, 31–41 (2011).
Corley, D. A., Kerlikowske, K., Verma, R. & Buffler, P. Protective association of aspirin/NSAIDs and esophageal cancer: a systematic review and meta-analysis. Gastroenterology 124, 47–56 (2003).
Vaughan, T. L. et al. Non-steroidal anti-inflammatory drugs and risk of neoplastic progression in Barrett's oesophagus: a prospective study. Lancet Oncol. 6, 945–952 (2005).
Kostadinov, R. L. et al. NSAIDs Modulate Clonal Evolution in Barrett's Esophagus. PLoS Genet. 9, e1003553 (2013).
Parry, G. D. The meaning of r- and K-selection. Oecol. (Berlin) 48, 260–264 (1981).
Mueller, L. D. Density-dependent population growth and natural selection in food-limited environments: The Drosophila model. Am. Nat. 132, 786–809 (1988).
Levins, R. Evolution in Changing Environments (Princeton Univ. Press, 1968).
Gatenby, R. A., Grove, O. & Gillies, R. J. Quantitative imaging in cancer evolution and ecology. Radiology 269, 8–14 (2013)
Acknowledgements
The authors thank A. Nedelcu, A. Caulin and A. J. Figuredo for thoughtful and thought-provoking discussions during the development of these ideas. This work was supported in part by Research Scholar Grant number 117209-RSG-09-163-01-CNE from the American Cancer Society, by US National Institutes of Health (NIH) grants F32 CA144331, R01 CA149566, R01 CA170595, R01 CA140657 and U54 CA143970, and by a grant from the McDonnell Foundation 220020270.
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Aktipis, C., Boddy, A., Gatenby, R. et al. Life history trade-offs in cancer evolution. Nat Rev Cancer 13, 883–892 (2013). https://doi.org/10.1038/nrc3606
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DOI: https://doi.org/10.1038/nrc3606
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