Journal of Molecular Medicine

, Volume 90, Issue 5, pp 509–522 | Cite as

Evolutionary molecular medicine

  • Randolph M. Nesse
  • Detlev Ganten
  • T. Ryan Gregory
  • Gilbert S. Omenn
Review

Abstract

Evolution has long provided a foundation for population genetics, but some major advances in evolutionary biology from the twentieth century that provide foundations for evolutionary medicine are only now being applied in molecular medicine. They include the need for both proximate and evolutionary explanations, kin selection, evolutionary models for cooperation, competition between alleles, co-evolution, and new strategies for tracing phylogenies and identifying signals of selection. Recent advances in genomics are transforming evolutionary biology in ways that create even more opportunities for progress at its interfaces with genetics, medicine, and public health. This article reviews 15 evolutionary principles and their applications in molecular medicine in hopes that readers will use them and related principles to speed the development of evolutionary molecular medicine.

Keywords

Evolution Biology Genetics Darwinian medicine Evolutionary medicine Evolutionary molecular medicine 

References

  1. 1.
    Nesse RM, Williams GC (1994) Why we get sick: the new science of Darwinian medicine. Times Books, New YorkGoogle Scholar
  2. 2.
    Williams GC, Nesse RM (1991) The dawn of Darwinian medicine. Q Rev Biol 66:1–22PubMedCrossRefGoogle Scholar
  3. 3.
    Nesse RM, Stearns SC (2008) The great opportunity: evolutionary applications to medicine and public health. Evol Appl 1:28–48CrossRefGoogle Scholar
  4. 4.
    Stearns SC (ed) (1999) Evolution in health and disease. Oxford University Press, OxfordGoogle Scholar
  5. 5.
    Gluckman P, Beedle A, Hanson M (2009) Principles of evolutionary medicine. Oxford University Press, OxfordGoogle Scholar
  6. 6.
    Stearns SC, Koella JC (eds) (2008) Evolution in health and disease, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  7. 7.
    Perlman RL (2011) Evolutionary biology: a basic science for medicine in the 21st century. Perspect Biol Med 54:75–88. doi:10.1353/pbm.2011.0012 PubMedCrossRefGoogle Scholar
  8. 8.
    Gregory TR (2008) The evolution of complex organs. Evol: Educ Outreach 1:358–389CrossRefGoogle Scholar
  9. 9.
    Orr HA (2009) Fitness and its role in evolutionary genetics. Nat Rev Genet 10:531–539PubMedCrossRefGoogle Scholar
  10. 10.
    Weiss KM, Buchanan A (2004) Genetics and the logic of evolution. Wiley-Liss, HobokenCrossRefGoogle Scholar
  11. 11.
    Maynard Smith J (1998) Evolutionary genetics, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  12. 12.
    Crespi BJ (2011) The emergence of human-evolutionary medical genomics. Evolutionary Applications 4:292–314. doi:10.1111/j.1752-4571.2010.00156.x CrossRefGoogle Scholar
  13. 13.
    Fox CW, Wolf JB (2006) Evolutionary genetics: concepts and case studies. Oxford University Press, New YorkGoogle Scholar
  14. 14.
    Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407PubMedCrossRefGoogle Scholar
  15. 15.
    Finch CE, Sapolsky RM (1999) The evolution of alzheimer disease, the reproductive schedule, and apoe isoforms. Neurobiol Aging 20:407–428PubMedCrossRefGoogle Scholar
  16. 16.
    Childs B (1999) Genetic medicine: a logic of disease. Johns Hopkins University Press, BaltimoreGoogle Scholar
  17. 17.
    Childs B, Wiener C, Valle D (2005) A science of the individual: implications for a medical school curriculum. Annu Rev Genomics Hum Genet 6:313–330PubMedCrossRefGoogle Scholar
  18. 18.
    Nesse RM, Dawkins R (2010) Evolution: medicine’s most basic science. In: Warrell DA, Cox TM, Firth JD, Benz EJJ (eds) Oxford textbook of medicine, 5th edn. Oxford University Press, Oxford, pp 12–15Google Scholar
  19. 19.
    Nesse RM, Bergstrom CT, Ellison PT, Flier JS, Gluckman P, Govindaraju DR, Niethammer D, Omenn GS, Perlman RL, Schwartz MD et al (2010) Making evolutionary biology a basic science for medicine. Proc Natl Acad Sci USA 107(Suppl 1):1800–1807. doi:10.1073/pnas.0906224106 PubMedCrossRefGoogle Scholar
  20. 20.
    Nesse RM (2005) Maladaptation and natural selection. Q Rev Biol 80:62–70PubMedCrossRefGoogle Scholar
  21. 21.
    Eaton SB, Cordain L, Eaton SB III (2001) An evolutionary foundation for health promotion. World Rev Nutr Diet 90:5–12PubMedCrossRefGoogle Scholar
  22. 22.
    Eaton SB, Strassman BI, Nesse RM, Neel JV, Ewald PW, Williams GC, Weder AB, Eaton SB III, Lindeberg S, Konner MJ et al (2002) Evolutionary health promotion. Prev Med 34:109–118PubMedCrossRefGoogle Scholar
  23. 23.
    Rook G (ed) (2009) The hygiene hypothesis and Darwinian medicine. Birkhauser Basel, BostonGoogle Scholar
  24. 24.
    Correale J, Farez M (2007) Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol 61:97–108PubMedCrossRefGoogle Scholar
  25. 25.
    Elliott DE, Summers RW, Weinstock JV (2007) Helminths as governors of immune-mediated inflammation. Int J Parasit 37:457–464CrossRefGoogle Scholar
  26. 26.
    Keller TL, Zocco D, Sundrud MS, Hendrick M, Edenius M, Yum J, Kim YJ, Lee HK, Cortese JF, Wirth DF et al (2012) Halofuginone and other febrifugine derivatives inhibit prolyl-trna synthetase. Nat Chem Biol 8:311–317. doi:10.1038/nchembio.790 PubMedCrossRefGoogle Scholar
  27. 27.
    Nesse RM, Berridge KC (1997) Psychoactive drug use in evolutionary perspective. Science 278:63–66PubMedCrossRefGoogle Scholar
  28. 28.
    Weiss KM (2008) Tilting at quixotic trait loci (QTL): an evolutionary perspective on genetic causation. Genetics 179:1741–1756. doi:10.1534/genetics.108.094128 PubMedCrossRefGoogle Scholar
  29. 29.
    Bulik CM, Sullivan PF, Tozzi F, Furberg H, Lichtenstein P, Pedersen NL (2006) Prevalence, heritability, and prospective risk factors for anorexia nervosa. Arch Gen Psychiatry 63:305–312. doi:10.1001/archpsyc.63.3.305 PubMedCrossRefGoogle Scholar
  30. 30.
    Turkheimer E (1991) Individual and group differences in adoption studies of IQ. Psychol Bull 110:392–405CrossRefGoogle Scholar
  31. 31.
    Holmes EC (2004) Adaptation and immunity. PLoS Biol 2:e307PubMedCrossRefGoogle Scholar
  32. 32.
    Contreras-Galindo R, Kaplan MH, Leissner P, Verjat T, Ferlenghi I, Bagnoli F, Giusti F, Dosik MH, Hayes DF, Gitlin SD et al (2008) Human endogenous retrovirus k (HML-2) elements in the plasma of people with lymphoma and breast cancer. J Virol 82:9329–9336. doi:10.1128/JVI.00646-08 PubMedCrossRefGoogle Scholar
  33. 33.
    Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, USAGoogle Scholar
  34. 34.
    Finch CE (2009) Evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. Proc Natl Acad Sci USA 107(Suppl 1):1718–1724. doi:10.1073/pnas.0909606106 PubMedGoogle Scholar
  35. 35.
    Turke PW (2008) Williams's theory of the evolution of senescence: still useful at fifty. Q Rev Biol 83:243–256PubMedCrossRefGoogle Scholar
  36. 36.
    Zuk M, Bryant MJ, Kolluru GR, Mirmovitch V (1996) Trade-offs in parasitology, evolution and behavior. Parasitol Today 12:46–47PubMedCrossRefGoogle Scholar
  37. 37.
    Stearns S (1989) Trade-offs in life-history evolution. Funct Ecol 3(3):259–268CrossRefGoogle Scholar
  38. 38.
    Ellison PT (2001) On fertile ground. Harvard University Press, CambridgeGoogle Scholar
  39. 39.
    Kruger DJ, Nesse RM (2006) An evolutionary life-history framework for understanding sex differences in human mortality rates. Hum Nat 17:74–97CrossRefGoogle Scholar
  40. 40.
    Kruger D, Nesse RM (2004) Sexual selection and the male: female mortality ratio. Evol Psychol 2:66–85Google Scholar
  41. 41.
    Nesse RM (2005) Natural selection and the regulation of defenses: a signal detection analysis of the smoke detector principle. Evol Hum Behav 26:88–105CrossRefGoogle Scholar
  42. 42.
    Ellis BJ, Jackson JJ, Boyce WT (2006) The stress response systems: universality and adaptive individual differences. Dev Rev 26:175–212CrossRefGoogle Scholar
  43. 43.
    McEwen BS, Stellar E (1993) Stress and the individual: mechanisms leading to disease. Arch Intern Med 153:2093–2101. doi:10.1001/archinte.1993.00410180039004 PubMedCrossRefGoogle Scholar
  44. 44.
    Buss D, Haselton M, Shackelford T, Bleske A, Wakefield J (1998) Adaptations, exaptations, and spandrels. Am Psychol 53:533PubMedCrossRefGoogle Scholar
  45. 45.
    Nesse RM (2011) Ten questions for evolutionary studies of disease vulnerability. Evolutionary Applications 4:264–277. doi:10.1111/j.1752-4571.2010.00181.x CrossRefGoogle Scholar
  46. 46.
    Nesse RM, Weder A (2007) Darwinian medicine: What evolutionary medicine offers to endothelium researchers. In: Aird W (ed) Endothelial biomedicine. Cambridge University Press, Cambridge, pp 122–128CrossRefGoogle Scholar
  47. 47.
    Williams GC (1966) Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press, PrincetonGoogle Scholar
  48. 48.
    Dawkins R (1989) The selfish gene. New edition. Oxford University Press, OxfordGoogle Scholar
  49. 49.
    Wynne-Edwards VC (1962) Animal dispersion in relation to social behavior. Oliver and Boyd, EdinburghGoogle Scholar
  50. 50.
    Fischer O, Schmid-Hempel P (2005) Selection by parasites may increase host recombination frequency. Biol Lett 1:193–195. doi:10.1098/rsbl.2005.0296 PubMedCrossRefGoogle Scholar
  51. 51.
    West SA, El Mouden C, Gardner A (2011) Sixteen common misconceptions about the evolution of cooperation in humans. Evol Human Behav 32:231–262CrossRefGoogle Scholar
  52. 52.
    West SA, Griffin AS, Gardner A, Diggle SP (2006) Social evolution theory for microorganisms. Nat Rev Microbiol 4:597–607PubMedCrossRefGoogle Scholar
  53. 53.
    Frank SA (2012) Natural selection. III. Selection versus transmission and the levels of selection. J Evol Biol 25:227–243. doi:10.1111/j.1420-9101.2011.02431.x PubMedCrossRefGoogle Scholar
  54. 54.
    Wade MJ, Wilson DS, Goodnight C, Taylor D, Bar-Yam Y, de Aguiar MAM, Stacey B, Werfel J, Hoelzer GA, Brodie Iii ED et al (2010) Multilevel and kin selection in a connected world. Nature 463:E8–E9PubMedCrossRefGoogle Scholar
  55. 55.
    Hamilton WD (1964) The genetical evolution of social behavior I, and II. J Theor Biol 7:1–52PubMedCrossRefGoogle Scholar
  56. 56.
    Trivers RL (1985) Social evolution. Benjamin/Cummings, Menlo ParkGoogle Scholar
  57. 57.
    Alcock J (2001) The triumph of sociobiology. Oxford University Press, New YorkGoogle Scholar
  58. 58.
    Daly M, Wilson M (1995) Discriminative parental solicitude and the relevance of evolutionary models to the analysis of motivational systems. In: Gazzaniga M (ed) The cognitive neurosciences. The MIT Press, Cambridge, pp 1269–1286Google Scholar
  59. 59.
    Hawkes K, O'Connell JF, Blurton Jones NG, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA 95:1336–1339PubMedCrossRefGoogle Scholar
  60. 60.
    Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411CrossRefGoogle Scholar
  61. 61.
    Shanley D, Sear R, Mace R, Kirkwood T (2007) Testing evolutionary theories of menopause. Proc R Soc Lond B Biol Sci 274:2943–2949CrossRefGoogle Scholar
  62. 62.
    Hurst LD (1998) Selfish genes and meiotic drive. Nature 391:223. doi:10.1038/34523 PubMedCrossRefGoogle Scholar
  63. 63.
    Haig D, Grafen A (1991) Genetic scrambling as a defence against meiotic drive*. J Theor Biol 153:531–558PubMedCrossRefGoogle Scholar
  64. 64.
    Rose M, Oakley T (2007) The new biology: beyond the modern synthesis. Biol Direct 2:30PubMedCrossRefGoogle Scholar
  65. 65.
    Wilkins JF, Haig D (2003) What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4:359–368PubMedCrossRefGoogle Scholar
  66. 66.
    Burt A, Trivers R (2006) Genes in conflict: the biology of selfish genetic elements. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  67. 67.
    Partridge L, Hurst LD (1998) Sex and conflict. Science 281:2003–2008PubMedCrossRefGoogle Scholar
  68. 68.
    Hurst GDD, Hurst LD, Johnstone RA (1992) Intranuclear conflict and its role in evolution. Trends Ecol Evol 7:373–378. doi:10.1016/0169-5347(92)90007-x PubMedCrossRefGoogle Scholar
  69. 69.
    Turan N, Katari S, Gerson LF, Chalian R, Foster MW, Gaughan JP, Coutifaris C, Sapienza C (2010) Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology. PLoS Genet 6:e1001033. doi:10.1371/journal.pgen.1001033 PubMedCrossRefGoogle Scholar
  70. 70.
    Omenn GS, Yocum AK, Menon R (2010) Alternative splice variants, a new class of protein cancer biomarker candidates: findings in pancreatic cancer and breast cancer with systems biology implications. Dis Markers 28:241–251PubMedGoogle Scholar
  71. 71.
    Menon R, Roy A, Mukherjee S, Belkin S, Zhang Y, Omenn GS (2011) Functional implications of structural predictions for alternative splice proteins expressed in her2/neu-induced breast cancers. J Proteome Res 10:5503–5511. doi:10.1021/pr200772w PubMedGoogle Scholar
  72. 72.
    Hamilton WD (1966) The moulding of senescence by natural selection. J Theor Biol 12:12–45PubMedCrossRefGoogle Scholar
  73. 73.
    Kirkwood TBL, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond B Biol Sci 332:15–24PubMedCrossRefGoogle Scholar
  74. 74.
    Finch CE (2007) The biology of human longevity: Inflammation, nutrition, and aging in the evolution of lifespans. Academic, AmsterdamGoogle Scholar
  75. 75.
    Masoro EJ, Austad SN (2001) Handbook of the biology of aging, 5th edn. Academic, San DiegoGoogle Scholar
  76. 76.
    Kirkwood TB (2005) Understanding the odd science of aging. Cell 120:437–447. doi:10.1016/j.cell.2005.01.027 PubMedCrossRefGoogle Scholar
  77. 77.
    Austad SN (1998) Theories of aging: an overview. Aging (Milano) 10:146–147Google Scholar
  78. 78.
    Rose MR (1991) The evolutionary biology of aging. Oxford University Press, OxfordGoogle Scholar
  79. 79.
    Kenyon C (2011) The first long-lived mutants: discovery of the insulin/IGF-1 pathway for ageing. Philos Trans R Soc Lond B Biol Sci 366:9–16. doi:10.1098/rstb.2010.0276 PubMedCrossRefGoogle Scholar
  80. 80.
    Partridge L (2010) The new biology of ageing. Philos Trans R Soc Lond B Biol Sci 365:147–154. doi:10.1098/rstb.2009.0222 PubMedCrossRefGoogle Scholar
  81. 81.
    Crespi BJ (2010) The origins and evolution of genetic disease risk in modern humans. Ann N Y Acad Sci 1206:80–109. doi:10.1111/j.1749-6632.2010.05707.x PubMedCrossRefGoogle Scholar
  82. 82.
    Akinsheye I, Alsultan A, Solovieff N, Ngo D, Baldwin CT, Sebastiani P, Chui DHK, Steinberg MH (2011) Fetal hemoglobin in sickle cell anemia. Blood 118:19–27. doi:10.1182/blood-2011-03-325258 PubMedCrossRefGoogle Scholar
  83. 83.
    Battaglino R, Fu J, Späte U, Ersoy U, Joe M, Sedaghat L, Stashenko P (2004) Serotonin regulates osteoclast differentiation through its transporter. J Bone Miner Res 19:1420–1431. doi:10.1359/jbmr.040606 PubMedCrossRefGoogle Scholar
  84. 84.
    Power ML, Schulkin J (2009) The evolution of obesity. Johns Hopkins University Press, BaltimoreGoogle Scholar
  85. 85.
    Nesse RM, Bhatnagar S, Young EA (2007) Evolutionary origins and functions of the stress response. In: Fink G (ed) Encyclopedia of stress, 2nd edn. Academic, San Diego, pp 965–970CrossRefGoogle Scholar
  86. 86.
    Gemmell NJ, Slate J (2006) Heterozygote advantage for fecundity. PLoS One 1:e125. doi:10.1371/journal.pone.0000125 PubMedCrossRefGoogle Scholar
  87. 87.
    Andrés AM, Hubisz MJ, Indap A, Torgerson DG, Degenhardt JD, Boyko AR, Gutenkunst RN, White TJ, Green ED, Bustamante CD et al (2009) Targets of balancing selection in the human genome. Mol Biol Evol 26:2755–2764. doi:10.1093/molbev/msp190 PubMedCrossRefGoogle Scholar
  88. 88.
    Sanfilippo PG, Hewitt AW, Hammond CJ, Mackey DA (2010) The heritability of ocular traits. Surv Ophthalmol 55:561–583. doi:10.1016/j.survophthal.2010.07.003 PubMedCrossRefGoogle Scholar
  89. 89.
    Proctor RN (1988) Racial hygiene: medicine under the Nazis. Harvard University Press, CambridgeGoogle Scholar
  90. 90.
    Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, Silverman JS, Powell K, Mortensen HM, Hirbo JB, Osman M et al (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39:31–40PubMedCrossRefGoogle Scholar
  91. 91.
    Ingram C, Mulcare C, Itan Y, Thomas M, Swallow D (2009) Lactose digestion and the evolutionary genetics of lactase persistence. Hum Genet 124:579–591PubMedCrossRefGoogle Scholar
  92. 92.
    Beall CM (2007) Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA 104:8655–8660. doi:10.1073/pnas.0701985104 PubMedCrossRefGoogle Scholar
  93. 93.
    Omenn GS (2010) Evolution and public health. Proc Natl Acad Sci USA 107:1702–1709. doi:10.1073/pnas.0906198106 PubMedCrossRefGoogle Scholar
  94. 94.
    Jablonski NG (2004) The evolution of human skin and skin color. Annu Rev Anthrop 33:585–623CrossRefGoogle Scholar
  95. 95.
    Stephens JC, Reich DE, Goldstein DB, Shin HD, Smith MW, Carrington M, Winkler C, Huttley GA, Allikmets R, Schriml L et al (1998) Dating the origin of the CCR5-î32 AIDS-resistance allele by the coalescence of haplotypes. Am J Hum Genet 62:1507–1515PubMedCrossRefGoogle Scholar
  96. 96.
    Mecsas J, Franklin G, Kuziel WA, Brubaker RR, Falkow S, Mosier DE (2004) Evolutionary genetics: CCR5 mutation and plague protection. Nature 427:606–606PubMedCrossRefGoogle Scholar
  97. 97.
    Sabeti PC, Walsh E, Schaffner SF, Varilly P, Fry B, Hutcheson HB, Cullen M, Mikkelsen TS, Roy J, Patterson N et al (2005) The case for selection at CCR5-delta32. PLoS Biol 3:e378. doi:10.1371/journal.pbio.0030378 PubMedCrossRefGoogle Scholar
  98. 98.
    Cochran G, Hardy J, Harpending H (2006) Natural history of Ashkenazi intelligence. J Biosoc Sci 38:659–693. doi:10.1017/S0021932005027069 PubMedCrossRefGoogle Scholar
  99. 99.
    Bray SM, Mulle JG, Dodd AF, Pulver AE, Wooding S, Warren ST (2010) Signatures of founder effects, admixture, and selection in the Ashkenazi Jewish population. Proc Natl Acad Sci USA 107:16222–16227. doi:10.1073/pnas.1004381107 PubMedCrossRefGoogle Scholar
  100. 100.
    Risch N, Tang H, Katzenstein H, Ekstein J (2003) Geographic distribution of disease mutations in the Ashkenazi Jewish population supports genetic drift over selection. Am J Hum Genet 72:812–822PubMedCrossRefGoogle Scholar
  101. 101.
    Pierce SB, Spurrell CH, Mandell JB, Lee MK, Zeligson S, Bereman MS, Stray SM, Fokstuen S, MacCoss MJ, Levy-Lahad E et al (2011) Garrod's fourth inborn error of metabolism solved by the identification of mutations causing pentosuria. Proc Natl Acad Sci USA 108:18313–18317. doi:10.1073/pnas.1115888108 PubMedCrossRefGoogle Scholar
  102. 102.
    Gabriel SE, Brigman KN, Koller BH, Boucher RC, Stutts MJ (1994) Cystic fibrosis heterozygote resistance to cholera toxin in the cystic fibrosis mouse model. Science 266:107–109PubMedCrossRefGoogle Scholar
  103. 103.
    Pier G, Grout M, Zaidi T, Meluleni G, Mueschenborn S, Banting G, Ratcliff R, Evans M, Colledge W (1998) Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393:79–82PubMedCrossRefGoogle Scholar
  104. 104.
    Poolman EM, Galvani AP (2007) Evaluating candidate agents of selective pressure for cystic fibrosis. J R Soc Interface 4:91–98. doi:10.1098/rsif.2006.0154 PubMedCrossRefGoogle Scholar
  105. 105.
    Eaton SB, Eaton SB III (2000) Paleolithic vs. modern diets—selected pathophysiological implications. Eur J Nutr 39:67–70. doi:10.1007/s003940070032 PubMedCrossRefGoogle Scholar
  106. 106.
    De Groot NG, Otting N, Doxiadis GGM, Balla-Jhagjhoorsingh SS, Heeney JL, Van Rood JJ, Gagneux P, Bontrop RE (2002) Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc Natl Acad Sci USA 99:11748–11753PubMedCrossRefGoogle Scholar
  107. 107.
    Barreiro LB, Quintana-Murci L (2010) From evolutionary genetics to human immunology: how selection shapes host defence genes. Nat Rev Genet 11:17–30PubMedCrossRefGoogle Scholar
  108. 108.
    Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES (2006) Positive natural selection in the human lineage. Science 312:1614–1620. doi:10.1126/science.1124309 PubMedCrossRefGoogle Scholar
  109. 109.
    Mallick S, Gnerre S, Muller P, Reich D (2009) The difficulty of avoiding false positives in genome scans for natural selection. Genome Res 19:922–933. doi:10.1101/gr.086512.108 PubMedCrossRefGoogle Scholar
  110. 110.
    Nielsen R, Hellmann I, Hubisz M, Bustamante C, Clark AG (2007) Recent and ongoing selection in the human genome. Nat Rev Genet 8:857–868PubMedCrossRefGoogle Scholar
  111. 111.
    Pickrell JK, Coop G, Novembre J, Kudaravalli S, Li JZ, Absher D, Srinivasan BS, Barsh GS, Myers RM, Feldman MW et al (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19:826–837. doi:10.1101/gr.087577.108 PubMedCrossRefGoogle Scholar
  112. 112.
    Pritchard JK, Di Rienzo A (2010) Adaptation—not by sweeps alone. Nat Rev Genet 11:665–667PubMedCrossRefGoogle Scholar
  113. 113.
    Ding Y, Larson G, Rivas G, Lundberg C, Geller L, Ouyang C, Weitzel J, Archambeau J, Slater J, Daly MB et al (2008) Strong signature of natural selection within an fhit intron implicated in prostate cancer risk. PLoS One 3:e3533. doi:10.1371/journal.pone.0003533 PubMedCrossRefGoogle Scholar
  114. 114.
    Lango Allen H, Estrada K, Lettre G, Berndt SI, Weedon MN, Rivadeneira F, Willer CJ, Jackson AU, Vedantam S, Raychaudhuri S et al (2010) Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467:832–838PubMedCrossRefGoogle Scholar
  115. 115.
    Omenn GS (2010) Overview of the symposium on public health significance of genomics and eco-genetics. Annu Rev Public Health 31:1–8. doi:10.1146/annurev.publhealth.012809.103639 PubMedCrossRefGoogle Scholar
  116. 116.
    Akil H, Brenner S, Kandel E, Kendler KS, King MC, Scolnick E, Watson JD, Zoghbi HY (2010) Medicine. The future of psychiatric research: genomes and neural circuits. Science 327:1580–1581. doi:10.1126/science.1188654 PubMedCrossRefGoogle Scholar
  117. 117.
    Cotton RGH, Auerbach AD, Axton M, Barash CI, Berkovic SF, Brookes AJ, Burn J, Cutting G, den Dunnen JT, Flicek P et al (2008) The human variome project. Science 322:861–862. doi:10.1126/science.1167363 PubMedCrossRefGoogle Scholar
  118. 118.
    Nesse RM (2009) Explaining depression: neuroscience is not enough, evolution is essential. In: Pariente CM, Nesse RM, Nutt DJ, Wolpert L (eds) Understanding depression: a translational approach. Oxford University Press, Oxford, pp 17–35Google Scholar
  119. 119.
    Nesse RM, Stein DJ (2012) Towards a genuinely medical model for psychiatric nosology. BMC Med 10:5. doi:10.1186/1741-7015-10-5 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Randolph M. Nesse
    • 1
  • Detlev Ganten
    • 2
  • T. Ryan Gregory
    • 3
  • Gilbert S. Omenn
    • 4
  1. 1.Detrainments of Psychiatry and PsychologyThe University of MichiganAnn ArborUSA
  2. 2.Charite-Universitätsmedizin BerlinMax Delbrück Center for Molecular Medicine (MDC)BerlinGermany
  3. 3.Department of Integrative BiologyUniversity of GuelphGuelphCanada
  4. 4.Center for Computational Medicine and BioinformaticsUniversity of MichiganAnn ArborUSA

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