1932

Abstract

Although tumorigenesis has been accepted as an evolutionary process (20, 102), many forces may operate differently in cancers than in organisms, as they evolve at vastly different time scales. Among such forces, natural selection, here defined as differential cellular proliferation among distinct somatic cell genotypes, is particularly interesting because its action might be thwarted in multicellular organisms (20, 29). In this review, selection is analyzed in two stages of cancer evolution: Stage I is the evolution between tumors and normal tissues, and Stage II is the evolution within tumors. The Cancer Genome Atlas (TCGA) data show a low degree of convergent evolution in Stage I, where genetic changes are not extensively shared among cases. An equally important, albeit much less highlighted, discovery using TCGA data is that there is almost no net selection in cancer evolution. Both positive and negative selection are evident but they neatly cancel each other out, rendering total selection ineffective in the absence of recombination. The efficacy of selection is even lower in Stage II, where neutral (non-Darwinian) evolution is increasingly supported by high-density sampling studies (81, 123). Because natural selection is not a strong deterministic force, cancers usually evolve divergently even in similar tissue environments.

[Erratum, Closure]

An erratum has been published for this article:
The Ecology and Evolution of Cancer: The Ultra-Microevolutionary Process
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2016-11-23
2024-04-20
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Literature Cited

  1. Abegglen LM, Caulin AF, Chan A, Lee K, Robinson R. 1.  et al. 2015. Potential mechanisms for cancer resistance in elephants and comparative cellular response to DNA damage in humans. JAMA 314:1850–60 [Google Scholar]
  2. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SAJR, Behjati S. 2.  et al. 2013. Signatures of mutational processes in human cancer. Nature 500:415–21 [Google Scholar]
  3. Almendro V, Marusyk A, Polyak K. 3.  2013. Cellular heterogeneity and molecular evolution in cancer. Annu. Rev. Pathol. Mech. Dis. 8:277–302 [Google Scholar]
  4. Amabile G, Di Ruscio A, Muller F, Welner RS, Yang H. 4.  et al. 2015. Dissecting the role of aberrant DNA methylation in human leukaemia. Nat. Commun. 6:7091 [Google Scholar]
  5. Babur Z, Gonen M, Aksoy BA, Schultz N, Ciriello G. 5.  et al. 2015. Systematic identification of cancer driving signaling pathways based on mutual exclusivity of genomic alterations. Genome Biol. 16:45 [Google Scholar]
  6. Barber LJ, Davies MN, Gerlinger M. 6.  2015. Dissecting cancer evolution at the macro-heterogeneity and micro-heterogeneity scale. Curr. Opin. Genet. Dev. 30:1–6 [Google Scholar]
  7. Bashashati A, Haffari G, Ding JR, Ha G, Lui K. 7.  et al. 2012. DriverNet: uncovering the impact of somatic driver mutations on transcriptional networks in cancer. Genome Biol 13:R124 [Google Scholar]
  8. Basil CF, Zhao YD, Zavaglia K, Jin P, Panelli MC. 8.  et al. 2006. Common cancer biomarkers. Cancer Res. 66:2953–61 [Google Scholar]
  9. Basu-Roy U, Bayin NS, Rattanakorn K, Han E, Placantonakis DG. 9.  et al. 2015. Sox2 antagonizes the Hippo pathway to maintain stemness in cancer cells. Nature Commun 6:6411 [Google Scholar]
  10. Beckman RA, Loeb LA. 10.  2005. Negative clonal selection in tumor evolution. Genetics 171:2123–31 [Google Scholar]
  11. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S. 11.  et al. 2010. The landscape of somatic copy-number alteration across human cancers. Nature 463:899–905 [Google Scholar]
  12. Bignell GR, Greenman CD, Davies H, Butler AP, Edkins S. 12.  et al. 2010. Signatures of mutation and selection in the cancer genome. Nature 463:893–98 [Google Scholar]
  13. Blighe K. 13.  2014. Cancer mutations and their tissue-specific nature. J. Cancer Sci. Ther. 6:9–11 [Google Scholar]
  14. Bodmer W. 14.  2008. Genetic instability is not a requirement for tumor development. Cancer Res. 68:3558–61 [Google Scholar]
  15. Bozic I, Antal T, Ohtsuki H, Carter H, Kim D. 15.  et al. 2013. Accumulation of driver and passenger mutations during tumor progression. PNAS 107:18545–50 [Google Scholar]
  16. Brock A, Krause S, Ingber DE. 16.  2015. Control of cancer formation by intrinsic genetic noise and microenvironmental cues. Nat. Rev. Cancer 15:499–509 [Google Scholar]
  17. Brocks D, Assenov Y, Minner S, Bogatyrova O, Simon R. 17.  et al. 2014. Intratumor DNA methylation heterogeneity reflects clonal evolution in aggressive prostate cancer. Cell Rep. 8:798–806 [Google Scholar]
  18. Burrell RA, McGranahan N, Bartek J, Swanton C. 18.  2013. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501:338–45 [Google Scholar]
  19. Cadieu E, Neff MW, Quignon P, Walsh K, Chase K. 19.  et al. 2009. Coat variation in the domestic dog is governed by variants in three genes. Science 326:150–53 [Google Scholar]
  20. Cairns J. 20.  1975. Mutation selection and the natural history of cancer. Nature 255:197–200 [Google Scholar]
  21. Caldas C. 21.  2012. Cancer sequencing unravels clonal evolution. Nat. Biotechnol. 30:408–10 [Google Scholar]
  22. Charlesworth B, Charlesworth D. 22.  2003. Evolution: A Very Short Introduction Oxford: Oxford Univ. Press145
  23. Charlesworth B, Charlesworth D. 23.  2010. Elements of Evolutionary Genetics Englewood, CO: Roberts Co. Publ.
  24. Chen H, Lin F, Xing K, He X. 24.  2015. The reverse evolution from multicellularity to unicellularity during carcinogenesis. Nat. Commun. 6:6367 [Google Scholar]
  25. Cheng X, Kao HY. 25.  2012. Post-translational modifications of PML: consequences and implications. Front. Oncol. 2:210 [Google Scholar]
  26. Chong CR, Jänne PA. 26.  2013. The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat. Med. 19:1389–400 [Google Scholar]
  27. Ciriello G, Miller ML, Aksoy BA, Senbabaoglu Y, Schultz N, Sander C. 27.  2013. Emerging landscape of oncogenic signatures across human cancers. Nat. Genet. 45:1127–33 [Google Scholar]
  28. 28. Consort. CSAA 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87 [Google Scholar]
  29. Crespi BJ, Summers K. 29.  2006. Positive selection in the evolution of cancer. Biol. Rev. Camb. Philos. Soc. 81:407–24 [Google Scholar]
  30. Crow JF, Kimura M. 30.  1970. An Introduction to Population Genetics Theory New York: Harper Row Publ.
  31. de Bruin EC, McGranahan N, Mitter R, Salm M, Wedge DC. 31.  et al. 2014. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 346:251–56 [Google Scholar]
  32. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC. 32.  et al. 2012. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 481:506–10 [Google Scholar]
  33. Durrett R. 33.  2013. Population genetics of neutral mutations in exponentially growing cancer cell populations. Ann. Appl. Probab. Off. J. Inst. Math. Stat. 23:230–50 [Google Scholar]
  34. Durrett R. 34.  2015. Branching Process Models of Cancer New York: Springer
  35. Dykhuizen D, Hartl DL. 35.  1980. Selective neutrality of 6PGD allozymes in E. coli and the effects of genetic background. Genetics 96:801–17 [Google Scholar]
  36. Eirew P, Steif A, Khattra J, Ha G, Yap D. 36.  et al. 2015. Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution. Nature 518:422–26 [Google Scholar]
  37. Ewens WJ. 37.  1972. The sampling theory of selectively neutral alleles. Theor. Popul. Biol. 3:87–112 [Google Scholar]
  38. Ewens WJ. 38.  2004. Mathematical Population Genetics New York: Springer
  39. Ewing AD, Houlahan KE, Hu Y, Ellrott K, Caloian C. 39.  et al. 2015. Combining tumor genome simulation with crowdsourcing to benchmark somatic single-nucleotide-variant detection. Nat. Methods 12:623–30 [Google Scholar]
  40. Fay JC, Wu CI. 40.  2000. Hitchhiking under positive Darwinian selection. Genetics 155:1405–13 [Google Scholar]
  41. Fearon ER, Vogelstein B. 41.  1990. A genetic model for colorectal tumorigenesis. Cell 61:759–67 [Google Scholar]
  42. Foll M, Gaggiotti OE, Daub JT, Vatsiou A, Excoffier L. 42.  2014. Widespread signals of convergent adaptation to high altitude in Asia and America. Am. J. Hum. Genet. 95:394–407 [Google Scholar]
  43. Fox EJ, Prindle MJ, Loeb LA. 43.  2013. Do mutator mutations fuel tumorigenesis?. Cancer Metastasis Rev 32:353–61 [Google Scholar]
  44. Fu YX. 44.  1996. New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–70 [Google Scholar]
  45. Fu YX, Li WH. 45.  1993. Statistical tests of neutrality of mutations. Genetics 133:693–709 [Google Scholar]
  46. Gajewski TF, Schreiber H, Fu Y-X. 46.  2013. Innate and adaptive immune cells in the tumor microenvironment. Nat. Immunol. 14:1014–22 [Google Scholar]
  47. Gatenby RA, Silva AS, Gillies RJ, Frieden BR. 47.  2009. Adaptive therapy. Cancer Res. 69:4894–903 [Google Scholar]
  48. Gerlinger M, Horswell S, Larkin J, Rowan AJ, Salm MP. 48.  et al. 2014. Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing. Nat. Genet. 46:225–33 [Google Scholar]
  49. Gerlinger M, McGranahan N, Dewhurst SM, Burrell RA, Tomlinson I, Swanton C. 49.  2014. Cancer: evolution within a lifetime. Annu. Rev. Genet. 48:215–36 [Google Scholar]
  50. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D. 50.  et al. 2012. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. New Engl. J. Med. 366:883–92 [Google Scholar]
  51. Gonzalez-Perez A, Perez-Llamas C, Deu-Pons J, Tamborero D, Schroeder MP. 51.  et al. 2013. IntOGen-mutations identifies cancer drivers across tumor types. Nat. Methods 10:1081–82 [Google Scholar]
  52. Gould SJ. 52.  1990. Wonderful Life: The Burgess Shale and the Nature of History New York: WW Norton
  53. Gould SJ, Lewontin RC. 53.  1979. Spandrels of San Marco and the Panglossian Paradigm: a critique of the adaptationist program. Proc. R. Soc. Ser. B 205:581–98 [Google Scholar]
  54. Greaves M, Maley CC. 54.  2012. Clonal evolution in cancer. Nature 481:306–13 [Google Scholar]
  55. Greenberg AJ, Moran JR, Coyne JA, Wu C-I. 55.  2003. Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302:1754–57 [Google Scholar]
  56. Greenberg AJ, Wu C-I. 56.  2006. Molecular genetics of natural populations. Mol. Biol. Evol. 23:883–86 [Google Scholar]
  57. Hanahan D, Weinberg RA. 57.  2011. Hallmarks of cancer: the next generation. Cell 144:646–74 [Google Scholar]
  58. Harris H. 58.  1971. Polymorphism and protein evolution. The neutral mutation–random drift hypothesis. J. Med. Genet. 8:444 [Google Scholar]
  59. Hartl DL, Clark AG. 59.  2006. Principle of Population Genetics Sunderland, MA: Sinauer Assoc.
  60. Helleday T, Eshtad S, Nik-Zainal S. 60.  2014. Mechanisms underlying mutational signatures in human cancers. Nat. Rev. Genet. 15:585–98 [Google Scholar]
  61. Hill WG, Robertson A. 61.  1966. The effect of linkage on limits to artificial selection. Genet. Res. 8:269–94 [Google Scholar]
  62. Hofree M, Shen JP, Carter H, Gross A, Ideker T. 62.  2013. Network-based stratification of tumor mutations. Nat. Methods 10:1108–15 [Google Scholar]
  63. Hudson RR, Kreitman M, Aguadé M. 63.  1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–59 [Google Scholar]
  64. Hughes AL. 64.  1999. Adaptive Evolution of Genes and Genomes New York: Oxford Univ. Press270
  65. Jacobsen A, Silber J, Harinath G, Huse JT, Schultz N, Sander C. 65.  2013. Analysis of microRNA-target interactions across diverse cancer types. Nat. Struct. Mol. Biol. 20:1325–32 [Google Scholar]
  66. Jones S, Chen W-D, Parmigiani G, Diehl F, Beerenwinkel N. 66.  et al. 2008. Comparative lesion sequencing provides insights into tumor evolution. PNAS 105:4283–88 [Google Scholar]
  67. Junttila MR, de Sauvage FJ. 67.  2013. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 501:346–54 [Google Scholar]
  68. Kandoth C, McLellan MD, Vandin F, Ye K, Niu B. 68.  et al. 2013. Mutational landscape and significance across 12 major cancer types. Nature 502:333–39 [Google Scholar]
  69. Kimura M. 69.  1968. Evolutionary rate at the molecular level. Nature 217:624–26 [Google Scholar]
  70. Kimura M. 70.  1983. The Neutral Theory of Molecular Evolution Cambridge: Cambridge Univ. Press
  71. King JL, Jukes TH. 71.  1969. Non-Darwinian evolution. Science 164:788–98 [Google Scholar]
  72. Kondrashov AS. 72.  1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336:435–40 [Google Scholar]
  73. Kreso A, O'Brien CA, van Galen P, Gan OI, Notta F. 73.  et al. 2013. Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 339:543–48 [Google Scholar]
  74. Lambert A. 74.  2009. The allelic partition for coalescent point processes. Markov Process. Relat. Fields 15:359–86 [Google Scholar]
  75. Lande R. 75.  1995. Mutation and conservation. Conserv. Biol. 9:782–91 [Google Scholar]
  76. Lawrence MS, Stojanov P, Mermel CH, Robinson JT, Garraway LA. 76.  et al. 2014. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 505:495–501 [Google Scholar]
  77. Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K. 77.  et al. 2013. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499:214–18 [Google Scholar]
  78. Lewontin RC, Hubby JL. 78.  1966. A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54:595 [Google Scholar]
  79. Li W-H. 79.  1997. Molecular Evolution Sunderland, MA: Sinauer Assoc487
  80. Li Y, Rogoff HA, Keates S, Gao Y, Murikipudi S. 80.  et al. 2015. Suppression of cancer relapse and metastasis by inhibiting cancer stemness. PNAS 112:1839–44 [Google Scholar]
  81. Ling S, Hu Z, Yang Z, Yang F, Li Y. 81.  et al. 2015. Extremely high genetic diversity in a single tumor points to prevalence of non-Darwinian cell evolution. PNAS 112:E6496–505 [Google Scholar]
  82. Lu J, Wu CI. 82.  2005. Weak selection revealed by the whole-genome comparison of the X chromosome and autosomes of human and chimpanzee. PNAS 102:4063–67 [Google Scholar]
  83. Lynch M, Bürger R, Butcher D, Gabriel W. 83.  1993. The mutational meltdown in asexual populations. J. Hered. 84:339–44 [Google Scholar]
  84. Malcikova J, Stano-Kozubik K, Tichy B, Kantorova B, Pavlova S. 84.  2015. Detailed analysis of therapy-driven clonal evolution of TP53 mutations in chronic lymphocytic leukemia. Leukemia 29:877–85 [Google Scholar]
  85. Malek JA, Martinez A, Mery E, Ferron G, Huang R. 85.  et al. 2012. Gene expression analysis of matched ovarian primary tumors and peritoneal metastasis. J. Transl. Med. 10:121 [Google Scholar]
  86. Maley CC, Galipeau PC, Finley JC, Wongsurawat VJ, Li X. 86.  et al. 2006. Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nat. Genet. 38:468–73 [Google Scholar]
  87. Martincorena I, Campbell PJ. 87.  2015. Somatic mutation in cancer and normal cells. Science 349:1483–89 [Google Scholar]
  88. Marusyk A, Almendro V, Polyak K. 88.  2012. Intra-tumour heterogeneity: a looking glass for cancer?. Nat. Rev. Cancer 12:323–34 [Google Scholar]
  89. McDonald JH, Kreitman MA. 89.  1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–54 [Google Scholar]
  90. McFarland CD, Korolev KS, Kryukov GV, Sunyaev SR, Mirny LA. 90.  2013. Impact of deleterious passenger mutations on cancer progression. PNAS 110:2910–15 [Google Scholar]
  91. McFarland CD, Yaglom JA, Wojtkowiak JW, Scott JG, Morse DL. 91.  et al. 2015. Passenger DNA alterations reduce cancer fitness in cell culture and mouse models. bioRxiv 2015:026302 [Google Scholar]
  92. McGranahan N, Swanton C. 92.  2015. Biological and therapeutic impact of intratumor heterogeneity in cancer evolution. Cancer Cell 27:15–26 [Google Scholar]
  93. Messer PW, Petrov DA. 93.  2013. Frequent adaptation and the McDonald-Kreitman test. PNAS 110:8615–20 [Google Scholar]
  94. Meyer RS, Purugganan MD. 94.  2013. Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14:840–52 [Google Scholar]
  95. Mitra K, Carvunis A-R, Ramesh SK, Ideker T. 95.  2013. Integrative approaches for finding modular structure in biological networks. Nat. Rev. Genet. 14:719–32 [Google Scholar]
  96. Moran PAP. 96.  1958. Random processes in genetics. Proc. Camb. Philos. Soc. 54:60–71 [Google Scholar]
  97. Morris SC. 97.  1998. The Crucible of Creation: The Burgess Shale and the Rise of Animals Oxford: Oxford Univ. Press
  98. Nagy JD, Victor EM, Cropper JH. 98.  2007. Why don't all whales have cancer? A novel hypothesis resolving Peto's paradox. Integr. Comp. Biol. 47:317–28 [Google Scholar]
  99. Nei M. 99.  1987. Molecular Evolutionary Genetics New York: Columbia Univ. Press
  100. Niederst MJ, Engelman JA. 100.  2013. Bypass mechanisms of resistance to receptor tyrosine kinase inhibition in lung cancer. Sci. Signal. 6:re6 [Google Scholar]
  101. Nowak MA, Michor F, Iwasa Y. 101.  2003. The linear process of somatic evolution. PNAS 100:14966–69 [Google Scholar]
  102. Nowell PC. 102.  1976. The clonal evolution of tumor cell populations. Science 194:23–28 [Google Scholar]
  103. Ortmann CA, Kent DG, Nangalia J, Silber Y, Wedge DC. 103.  et al. 2015. Effect of mutation order on myeloproliferative neoplasms. N. Engl. J. Med. 372:601–12 [Google Scholar]
  104. Ostrow SL, Barshir R, DeGregori J, Yeger-Lotem E, Hershberg R. 104.  2014. Cancer evolution is associated with pervasive positive selection on globally expressed genes. PLOS Genet 10:e1004239 [Google Scholar]
  105. Pardo EP, Godzik A. 105.  2015. Analysis of individual protein regions provides novel insights on cancer pharmacogenomics. PLOS Comput. Biol. 11:e1004024 [Google Scholar]
  106. Park SY, Gonen M, Kim HJ, Michor F, Polyak K. 106.  2010. Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype. J. Clin. Investig. 120:644 [Google Scholar]
  107. Parker J, Tsagkogeorga G, Cotton JA, Liu Y, Provero P. 107.  et al. 2013. Genome-wide signatures of convergent evolution in echolocating mammals. Nature 502:228–31 [Google Scholar]
  108. Paull EO, Carlin DE, Niepel M, Sorger PK, Haussler D, Stuart JM. 108.  2013. Discovering causal pathways linking genomic events to transcriptional states using tied diffusion through interacting events (TieDIE). Bioinformatics 29:2757–64 [Google Scholar]
  109. Plaks V, Kong N, Werb Z. 109.  2015. The cancer stem cell niche: How essential is the niche in regulating stemness of tumor cells?. Cell Stem Cell 16:225–38 [Google Scholar]
  110. Podlaha O, Riester M, De S, Michor F. 110.  2012. Evolution of the cancer genome. Trends Genet. 28:155–63 [Google Scholar]
  111. Porta-Pardo E, Godzik A. 111.  2014. e-Driver: a novel method to identify protein regions driving cancer. Bioinformatics 30:3109–14 [Google Scholar]
  112. Porta-Pardo E, Hrabe T, Godzik A. 112.  2015. A pan-cancer catalogue of driver protein interaction interfaces. PLOS Comput. Biol. 11:e1004518 [Google Scholar]
  113. Read AF, Day T, Huijben S. 113.  2011. The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy. PNAS 108:10871–77 [Google Scholar]
  114. Reimand J, Wagih O, Bader GD. 114.  2013. The mutational landscape of phosphorylation signaling in cancer. Sci. Rep. 3:2651 [Google Scholar]
  115. Rodrguez-Paredes M, Esteller M. 115.  2011. Cancer epigenetics reaches mainstream oncology. Nat. Med. 17:330–39 [Google Scholar]
  116. Sabeti PC, Reich DE, Higgins JM, Levine HZ, Richter DJ. 116.  et al. 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832–37 [Google Scholar]
  117. Schaefer MH, Serrano L. 117.  2016. Cell type–specific properties and environment shape tissue specificity of cancer genes. Sci. Rep. 6:20707 [Google Scholar]
  118. Shendure J, Akey JM. 118.  2015. The origins, determinants, and consequences of human mutations. Science 349:1478–83 [Google Scholar]
  119. Shibata D, Navidi W, Salovaara R, Li ZH, Aaltonen LA. 119.  1996. Somatic microsatellite mutations as molecular tumor clocks. Nat. Med. 2:676–81 [Google Scholar]
  120. Sieber OM, Tomlinson SR, Tomlinson IPM. 120.  2005. Tissue, cell and stage specificity of (epi)mutations in cancers. Nat. Rev. Cancer 5:649–55 [Google Scholar]
  121. Siegmund KD, Marjoram P, Tavaré S, Shibata D. 121.  2011. High DNA methylation pattern intratumoral diversity implies weak selection in many human colorectal cancers. PLOS ONE 6:e21657 [Google Scholar]
  122. Silva AS, Kam Y, Khin ZP, Minton SE, Gillies RJ, Gatenby RA. 122.  2012. Evolutionary approaches to prolong progression-free survival in breast cancer. Cancer Res 72:6362–70 [Google Scholar]
  123. Sottoriva A, Kang H, Ma Z, Graham TA, Salomon MP. 123.  et al. 2015. A Big Bang model of human colorectal tumor growth. Nat. Genet. 47:209–16 [Google Scholar]
  124. Sulak M, Fong L, Mika K, Chigurupati S, Yon L. 124.  et al. 2015. TP53 copy number expansion correlates with the evolution of increased body size and an enhanced DNA damage response in elephants. bioRxiv 2015:028522 [Google Scholar]
  125. Swanton C. 125.  2012. Intratumor heterogeneity: evolution through space and time. Cancer Res. 72:4875–82 [Google Scholar]
  126. Tabassum DP, Polyak K. 126.  2015. Tumorigenesis: It takes a village. Nat. Rev. Cancer 15:473–83 [Google Scholar]
  127. Tajima F. 127.  1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–95 [Google Scholar]
  128. Tamborero D, Gonzalez-Perez A, Perez-Llamas C, Deu-Pons J, Kandoth C. 128.  et al. 2013. Comprehensive identification of mutational cancer driver genes across 12 tumor types. Sci. Rep. 3:2650 [Google Scholar]
  129. Tao Y, Hu Z, Ling S, Yeh S-H, Zhai W. 129.  et al. 2015. Further genetic diversification in multiple tumors and an evolutionary perspective on therapeutics. bioRxiv 2015:025429 [Google Scholar]
  130. Tao Y, Ruan J, Yeh S-H, Lu X, Wang Y. 130.  et al. 2011. Rapid growth of a hepatocellular carcinoma and the driving mutations revealed by cell-population genetic analysis of whole-genome data. PNAS 108:12042–47 [Google Scholar]
  131. Tian X, Azpurua J, Hine C, Vaidya A, Myakishev-Rempel M. 131.  et al. 2013. High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat. Nature 499:346–49 [Google Scholar]
  132. Ting C-T, Takahashi A, Wu C-I. 132.  2001. Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci. PNAS 98:6709–13 [Google Scholar]
  133. Vandin F, Upfal E, Raphael BJ. 133.  2011. Algorithms for detecting significantly mutated pathways in cancer. J. Comput. Biol. 18:507–22 [Google Scholar]
  134. Vaske CJ, Benz SC, Sanborn JZ, Earl D, Szeto C. 134.  et al. 2010. Inference of patient-specific pathway activities from multi-dimensional cancer genomics data using PARADIGM. Bioinformatics 26:237–45 [Google Scholar]
  135. Vermeulen L, Morrissey E, van der Heijden M, Nicholson AM, Sottoriva A. 135.  et al. 2013. Defining stem cell dynamics in models of intestinal tumor initiation. Science 342:995–98 [Google Scholar]
  136. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA, Kinzler KW. 136.  2013. Cancer genome landscapes. Science 339:1546–58 [Google Scholar]
  137. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 137.  2006. A map of recent positive selection in the human genome. PLOS Biol. 4:e72 [Google Scholar]
  138. Vuong H, Cheng FX, Lin CC, Zhao ZM. 138.  2014. Functional consequences of somatic mutations in cancer using protein pocket–based prioritization approach. Genome Med 6:81 [Google Scholar]
  139. Waclaw B, Bozic I, Pittman ME, Hruban RH, Vogelstein B, Nowak MA. 139.  2015. A spatial model predicts that dispersal and cell turnover limit intratumour heterogeneity. Nature 525:261–64 [Google Scholar]
  140. Wakely J. 140.  2009. Coalescent Theory: An Introduction New York: WH Freeman
  141. Wang X, Jung Y-S, Jun S, Lee S, Wang W. 141.  et al. 2016. PAF-Wnt signaling–induced cell plasticity is required for maintenance of breast cancer cell stemness. Nat. Commun. 7:10633 [Google Scholar]
  142. Watson IR, Takahashi K, Futreal PA, Chin L. 142.  2013. Emerging patterns of somatic mutations in cancer. Nat. Rev. Genet. 14:703–18 [Google Scholar]
  143. Watterson GA. 143.  1978. The homozygosity test of neutrality. Genetics 88:405–17 [Google Scholar]
  144. Watterson GA. 144.  1984. Lines of descent and the coalescent. Theor. Popul. Biol. 26:77–92 [Google Scholar]
  145. Weisenberger DJ. 145.  2014. Characterizing DNA methylation alterations from The Cancer Genome Atlas. J. Clin. Investig. 124:17–23 [Google Scholar]
  146. Wilding J, Bodmer W. 146.  2015. Genetic instability. Oxford Textbook of Oncology DJ Kerr, DG Haller, CJH van de Velde, M Baumann 72–81 Oxford: Oxford Univ. Press [Google Scholar]
  147. Williams MJ, Werner B, Barnes CP, Graham TA, Sottoriva A. 147.  2016. Identification of neutral tumor evolution across cancer types. Nat. Genet. 48:238–44 [Google Scholar]
  148. Wu X, Kimmel M. 148.  2013. Modeling neutral evolution using an infinite-allele Markov branching process. Int. J. Stoch. Anal. 2013:963831 [Google Scholar]
  149. Yates LR, Campbell PJ. 149.  2012. Evolution of the cancer genome. Nat. Rev. Genet. 13:795–806 [Google Scholar]
  150. Zack TI, Schumacher SE, Carter SL, Cherniack AD, Saksena G. 150.  et al. 2013. Pan-cancer patterns of somatic copy number alteration. Nat. Genet. 45:1134–40 [Google Scholar]
  151. Zeng K, Shi S, Wu C-I. 151.  2007. Compound tests for the detection of hitchhiking under positive selection. Mol. Biol. Evol. 24:1898–908 [Google Scholar]
  152. Zhao JF, Cheng FX, Wang YY, Arteaga CL, Zhao ZM. 152.  2016. Systematic prioritization of druggable mutations in similar to 5000 genomes across 16 cancer types using a structural genomics-based approach. Mol. Cell. Proteom. 15:642–56 [Google Scholar]
  153. Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P. 153.  2012. Parallel molecular evolution in an herbivore community. Science 337:1634–37 [Google Scholar]
  154. Zhong S, Khodursky A, Dykhuixen DE, Dean AM. 154.  2004. Evolutionary genomics of ecological specialization. PNAS 101:11719–24 [Google Scholar]
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/content/journals/10.1146/annurev-genet-112414-054842
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  • Article Type: Review Article
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