From Genes to Numbers: Effective Population Sizes in Human Evolution

  • John Hawks

Abstract

The effective population size has become a central aspect of our understanding of the ancient structure of human populations. It is through this concept that the genetic variation of present-day humans may inform us about the number and relationships of humans in the past. However, effective population size itself is not a demographic parameter. If the theoretical model does not apply accurately to human evolution, then inferences based on the estimates of effective population size may be in error. Here, I present the theoretical basis of effective population size, including many of the demographic and evolutionary conditions that can confound the relationship of genetic variation and population size.

Keywords

Migration Europe Recombination Stratification Expense 

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References

  1. Austerlitz, F., Heyer, E., 1998. Social transmission of reproductive behavior increases frequency of inherited disorders in a young-expanding population. Proc. natl. Acad. Sci. USA. 95, 15140–15144.Google Scholar
  2. Ayala, F.J., 1995. The myth of eve: molecular biology and human origins. Science 270, 1930–1936.CrossRefGoogle Scholar
  3. Bamshad, M., Kivisild, T., Watkins, W.S., Dixon, M.E., Ricker, C.E., Rao, B.B., Naidu, J.M., Prasad, B.V.R., Reddy, P.G., Rasanayagam, A., Papiha, S.S., Villems, R., Redd, A.J., Hammer, M.F., Nguyen, S.V., Carroll, M.L., Batzer, M.A., Jorde, L.B., 2001. Genetic evidence on the origins of Indian caste populations. Genome. Res. 11, 994–1004.CrossRefGoogle Scholar
  4. Bazin, E., Glémin, S., Galtier, N., 2006. Population size does not influence mitochondrial genetic diversity in animals. Science 312, 570–572.CrossRefGoogle Scholar
  5. Beerli, P., Felsenstein, J., 2001. Maximum likelihood estimation of a migration matrix and effective population sizes in subpopulations by using a coalescent approach. Proc. natl. Acad. Sci. USA. 98, 4563–4568.Google Scholar
  6. Betancourt, A.J., Kim, Y., Orr, H.A., 2004. A pseudohitchhiking model of X vs. autosomal diversity. Genetics 168, 2261– 2269.CrossRefGoogle Scholar
  7. Biraben, J.-N., 1979. Essai sur l’evolution du nombre des hommes. Population 1, 13–25.CrossRefGoogle Scholar
  8. Birdsell, J.B., 1972. Human Evolution. Chicago: Rand McNally.Google Scholar
  9. Birdsell, J.B., 1993. Microevolutionary Patterns in Aboriginal Australia: A Gradient Analysis of Clines. Oxford University Press, Oxford, UK.Google Scholar
  10. Braverman, J.M., Hudson, R.R., Kaplan, N.L., Langley, C.H., Stephan, W., 1995. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140, 783–796.Google Scholar
  11. Cann, R.L., Stoneking, M., Wilson, A.C., 1987. Mitochondrial DNA and human evolution. Nature 325, 31–36.CrossRefGoogle Scholar
  12. Cannings, C., 1974. The latent roots of certain Markov chains arising in genetics: A new approach. 1. haploid models. Adv. in Appl. Probab. 6, 260–290.CrossRefGoogle Scholar
  13. Caspari, R., Lee, S.-H., 2004. Older age becomes common late in human evolution. Proc. natl. Acad. Sci. USA. 101, 10895– 10900.Google Scholar
  14. Cavalli-Sforza, L.L., 1959. Some data on the genetic structure of human populations. In: Proceedings of the 10th International Congress on Genetics, vol. 1. University of Toronto Press, Toronto, pp. 389–407.Google Scholar
  15. Charlesworth, B., Morgan, M., Charlesworth, D., 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303.Google Scholar
  16. Chen, Y.-S., Olckers, A., Schurr, T.G., Kogelnik, A.M., Huoponen, K., Wallace, D.C., 2000. mtDNA variation in the South African Kung and Khwe—and their genetic relationships to other African populations. Am. J. Hum. Genet. 66, 1362–1383.CrossRefGoogle Scholar
  17. Crow, J.F., Denniston, C., 1988. Inbreeding and variance effective numbers. Evolution 42, 482–495.CrossRefGoogle Scholar
  18. Eller, E., Hawks, J., Relethford, J.H., 2004. Local extinction and recolonization, species effective population size, and modern human origins. Hum. Biol. 76, 689–709.CrossRefGoogle Scholar
  19. Eswaran, V., 2002. A diffusion wave out of Africa: the mechanism of the modern human revolution? Curr. Anthropol. 43, 749– 774.CrossRefGoogle Scholar
  20. Evans, P.D., Mekel-Bobrov, N., Vallender, E.J., Hudson, R.R., Lahn, B.T., 2006. Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homolineage. Proc. natl. Acad. Sci. USA. Early online. doi:10.1073/pnas.0606966103.Google Scholar
  21. Ewens, W.J., 1972. The sampling theory of selectively neutral alleles. Theor. Pop. Biol. 3, 87–112.CrossRefGoogle Scholar
  22. Ewens, W.J., 2004. Mathematical Population Genetics. Cambridge University Press, Cambridge, UK.Google Scholar
  23. Fay, J.C., Wu, C.-I., 1999. A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol. Biol. Evol. 16, 1003– 1005.Google Scholar
  24. Fay, J.C., Wu, C.-I., 2000. Hitchhiking under positive darwinian selection. Genetics 155, 1405–1413.Google Scholar
  25. Fisher, R.A., 1918. The correlation between relatives on the supposition of Mendelian inheritance. Transactions of the Royal Society of Edinburgh 52, 399–433.Google Scholar
  26. Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford, Clarendon.Google Scholar
  27. Frayer, D.W., Wolpoff, M.H., Thorne, A.G., Smith, F.H., Pope, G.G., 1994. Getting it straight. Am. Anthrop. 96, 424– 438.CrossRefGoogle Scholar
  28. Fu, Y.X., Li, W.-H., 1997. Estimating the age of the common ancestor of a sample of DNA sequences. Mol. Biol. Evol. 14, 195–199.Google Scholar
  29. Gagnon, A., Heyer, E., 2001. Intergenerational correlation of effective family size in early (Québec Canada). Am. J. Hum. Biol. 13, 645–659.CrossRefGoogle Scholar
  30. Gamble, C., 1994. Timewalkers. The Prehistory of Global Colonization. Harvard University Press, Cambridge, MA.Google Scholar
  31. Gillespie, J.H., 2000. Genetic drift in an infinite population: the pseudohitchhiking model. Genetics 155, 909–919.Google Scholar
  32. Gillespie, J.H., 2001. Is the population size of a species relevant to its evolution? Evolution 55, 2161–2169.Google Scholar
  33. Gilpin, M., 1991. The genetic effective size of a metapopulation. Biological Journal of the Linnaean Society 42, 165–175.CrossRefGoogle Scholar
  34. Haigh, J., MaynardSmith, J., 1972. Population size and protein variation in man. Genet. Res. 19, 73–89.CrossRefGoogle Scholar
  35. Haldane, J.B.S., 1927. A mathematical theory of natural and artificial selection. Trans. Camb. Phil. Soc. 23, 19–41.Google Scholar
  36. Harpending, H., Rogers, A., 2000. Genetic perspectives on human origins and differentiation. Annu. Rev. of Genomics Hum. Genet. 1, 361–385.CrossRefGoogle Scholar
  37. Harpending, H.C., Batzer, M.A., Gurven, M., Jorde, L.B., Rogers, A.R., Sherry, S.T., 1998. Genetic traces of ancient demography. Proc. natl. Acad. Sci. USA. 95, 1961–1967.Google Scholar
  38. Harpending, H.C., Sherry, S.T., Rogers, A.R., Stoneking, M., 1993. The genetic structure of ancient human populations. Curr. Anthrop. 34, 483–496.CrossRefGoogle Scholar
  39. Hawks, J., Hunley, K., Lee, S.-H., Wolpoff, M.H., 2000. Bottlenecks and Pleistocene human evolution. Mol. Biol. Evol. 17, 2–22.Google Scholar
  40. Hawks, J.D., 1999. The Evolution of Human Population Size: A Synthesis of Fossil, Archaeological, and Genetic Data. Ph.D. thesis, University of Michigan, Ann Arbor.Google Scholar
  41. Hellmann, I., Ebersberger, I., Ptak, S.E., Pööbo, S., Przeworski, M., 2003. A neutral explanation for the correlation of diversity with recombination rates in humans. Am. J. hum. Genet. 72, 1527–1535.CrossRefGoogle Scholar
  42. Hill, W.G., 1972. Effective size of populations with overlapping generations. Theor. Pop. Biol. 3, 278–289.CrossRefGoogle Scholar
  43. Hudson, R.R., 1990. Gene genealogies and the coalescent process. Oxford Surveys in Evolutionary Biology 7, 1–44.Google Scholar
  44. Kim, Y., Stephan, W., 2000. Joint effects of genetic hitchhiking and background selection on neutral variation. Genetics 155, 1415–1427.Google Scholar
  45. Lehmann, L., Perrin, N., 2006. On metapopulation resistance to drift and extinction. Ecology 87, 1844–1855.CrossRefGoogle Scholar
  46. Levins, R., 1969. Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull. Entomological Society of America 71, 237–240.Google Scholar
  47. Marth, G., Schuler, G., Yeh, R., Davenport, R., Agarwala, R., Church, D., Wheelan, S., Baker, J., Ward, M., Kholodov, M., Phan, L., Czabarka, E., Murvai, J., Cutler, D., Wooding, S., Rogers, A., Chakravarti, A., Harpending, H.C., Kwok, P.-Y., Sherry, S.T., 2003. Sequence variations in the public human genome data reflect a bottlenecked population history. Proc. natl. Acad. Sci. USA. 100, 376–381.Google Scholar
  48. Marth, G.T., Czabarka, E., Murvai, J., Sherry, S.T., 2004. The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations. Genetics 166, 351–372.CrossRefGoogle Scholar
  49. Maruyama, T., Kimura, M., 1980. Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proc. natl. Acad. Sci. USA. 77, 6710–6714.Google Scholar
  50. Moran, P.A.P., 1958. Random Processes in Genetics. Proceedings of the Cambridge Philosophical Society 54, 60–71.Google Scholar
  51. Nachman, M.W., 2001. Single nucleotide polymorphisms and recombination rate in humans. Trends Genet. 17, 481–485.CrossRefGoogle Scholar
  52. Nachman, M.W., Bauer, V.L., Crowell, S.L., Aquadro, C.F., 1998. DNA variability and recombination rates at X-linked loci in humans. Genetics 150, 1133–1141.Google Scholar
  53. Nei, M., 1970. Effective size of human populations. Am. J. hum. Genet. 22, 694–696.Google Scholar
  54. Nei, M., Graur, D., 1984. Extent of protein polymorphism and the neutral mutation theory. Evol. Biol. 17, 73–118.Google Scholar
  55. Nei, M., Murata, M., 1966. Effective population size when fertility is inherited. Genet. Res. 8, 257–260.CrossRefGoogle Scholar
  56. Nei, M., Roychaudhury, A., 1982. Genetic relationship and evolution of human races. Evol. Biol. 14, 1–59.Google Scholar
  57. Nunney, L., 1993. The influence of mating system and overlapping generations on effective population size. Evolution 47, 1329–1341.CrossRefGoogle Scholar
  58. Nunney, L., Elam, D.R., 1994. Estimating the effective population size of conserved populations. Conserv. Biol. 8, 175–184.CrossRefGoogle Scholar
  59. Parra, E.J., Kittles, R.A., Argyropoulos, G., Pfaff, C.L., Hiester, K., Bonilla, C., Sylvester, N., Parrish-Gause, D., Garvey, W.T., Jin, L., McKeigue, P.M., Kamboh, M.I., Ferrell, R.E., Pollitzer, W.S., Shriver, M.D., 2001. Ancestral proportions and admixture dynamics in geographically defined African Americans living in South Carolina. Am. J. Phys. Anthropol. 114, 18–29. doi:10.1002/1096–8644(200101)114:1¡18::AID- AJPA1002¿3.0.CO;2–2.CrossRefGoogle Scholar
  60. Plagnol, V., Wall, J. D., 2006. Possible ancestral structure in human populations. PLoS Genet. 2:e105. doi:10:1371/journal.pgen.0020105.CrossRefGoogle Scholar
  61. Provine, W.B., 1971. The Origins of Theoretical Population Genetics. University of Chicago Press, Chicago.Google Scholar
  62. Sherry, S., Harpending, H., Batzer, M., Stoneking, M., 1997. Alu evolution in human populations: using the coalescent to estimate effective population size. Genetics 147, 1977–1982.Google Scholar
  63. Sibert, A., Austerlitz, A., Heyer, E. 2002., Wright-Fisher revisited: The case of fertility correlation. Theor. Pop. Biol. 62, 181–197.CrossRefGoogle Scholar
  64. Sjödin, P., Kaj, I., Krone, S., Lascoux, M., Nordborg, M., 2005. On the meaning and existence of an effective population size. Genetics 169, 1061–1070.CrossRefGoogle Scholar
  65. Stiner, M.C., Munro, N.D., Surovell, T.A., 2000. The tortoise and the hare: Small-game use, the broad-spectrum revolution, and Paleolithic demography. Curr. Anthrop. 41, 39–73.CrossRefGoogle Scholar
  66. Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis of DNA polymorphism. Genetics 123, 585- -595.Google Scholar
  67. Takahata, N., 1994. Repeated failures that led to the eventual success in human evolution. Mol. Biol. Evol. 11, 803–805.Google Scholar
  68. Takahata, N., Satta, Y., 1998. Footprints of intragenic recombination at HLA locus. Immunogenetics 47, 430–441.CrossRefGoogle Scholar
  69. Templeton, A.R., Read, B., 1994. Inbreeding: one word, several meanings, much confusion. In: Loeschcke, V., Tomiuk, J., Jain, S.K. (Eds.), Conservation Genetics. Birkhaduser Verlag, Basel, pp. 91–106.Google Scholar
  70. The International HapMap Consortium 2005. A haplotype map of the human genome. Nature 437, 1299–1320.CrossRefGoogle Scholar
  71. Tindale, N., 1940. Distribution of Australian aboriginal tribes: a field survey. Transactions of the Royal Society of South Australia 64, 140–231.Google Scholar
  72. Tishkoff, S.A., Williams, S.M., 2002. Genetic analysis of African populations: Human evolution and complex disease. Nat. Rev. Genet. 3, 611–621.CrossRefGoogle Scholar
  73. Underhill, P., Li, J., Lin, A.A., Mehdi, S.Q., Jenkins, T., Vollrath, D., Davis, R.W., Cavalli-Sforza, L., Oefner, P.J., 1997. Detection of numerous Y–chromosome biallelic polymorphisms by denaturing high-performance liquid chromatography. Genome Res. 7, 996–1005.Google Scholar
  74. Voight, B.F., Kudaravalli, S., Wen, X., Pritchard, J.K., 2006. A map of recent positive selection in the human genome. PLoS Biol. 4, e72. doi:10.1371/journal.pbio.0040072.CrossRefGoogle Scholar
  75. Wakeley, J., 2001. The coalescent in an island model of population subdivision with variation among demes. Theor. Pop. Biol. 59, 133–144.CrossRefGoogle Scholar
  76. Wall, J. D., Przeworski, M., 2000. When did the human population start increasing? Genetics 155, 1865–1874.Google Scholar
  77. Wang, D., Fan, J., Siao, C., Berno, A., Young, P., Sapolsky, R., Ghandour, G., Perkins, N., Winchester, E., Spencer, J., Kruglyak, L., Stein, L., Hsie, L., Topaloglou, T., Hubbell, E., Robinson, E., Mittmann, M., Morris, M., Shen, N., Kilburn, D., Rioux, J., Nusbaum, C., Rozen, S., Hudson, T., Lipshutz, R., Chee, M., Lander, E., 1998. Large-scale identification, mapping, and genotyping of single-nucleotide polymorphisms in the human genome. Science 280, 1077–1081.CrossRefGoogle Scholar
  78. Wang, E.T., Kodama, G., Baldi, P., Moyzis, R.K., 2006. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc. natl. Acad. Sci. USA. 103, 135–140.Google Scholar
  79. Weiss, K. 1984. On the number of members of the genus Homo who have ever lived, and some evolutionary implications. Hum. Biol. 56, 637–649.Google Scholar
  80. Whallon, R., 1989. Elements of cultural change in the later Paleolithic. In: Mellars, P., Stringer, C.B. (Eds.), The Human Revolution: Behavioural and Biological Perspectives on the Origins of Modern Humans. Edinburgh University Press, Edinburgh, pp. 433–454.Google Scholar
  81. Whitlock, M.C., Barton, N.H., 1997. The effective size of a subdivided population. Genetics 146, 427–441.Google Scholar
  82. Wolpoff, M.H., Hawks, J., Frayer, D.W., Hunley, K., 2001. Modern human ancestry at the peripheries: a test of the replacement theory. Science 291, 293–297.CrossRefGoogle Scholar
  83. Wood, J., 1987. The genetic demography of the Gainj of Papua New Guinea. 2. Determinates of effective population size. Am. Naturalist 129, 165–187.Google Scholar
  84. Wright, S., 1931. Evolution in mendelian populations. Genetics 16, 97–159.Google Scholar
  85. Wright, S., 1938. Size of a population and breeding structure in relation to evolution. Science 87, 430–431.Google Scholar
  86. Wright, S., 1943. Isolation by distance. Genetics 28, 114– 138.Google Scholar
  87. Wright, S., 1955. Classification of the factors of evolution. Cold Spring Harbor Symposia in Quantitative Biology 20, 16–24D.Google Scholar
  88. Yellen, J., Harpending, H., 1972. Hunter-gatherer populations and archaeological inference. World Archaeol. 4, 244–253.CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • John Hawks
    • 1
  1. 1.University of WisconsinUSA

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