When did the human population size start increasing? (original) (raw)

Abstract

We analyze the frequency spectra of all available human nuclear sequence data sets by using a model of constant population size followed by exponential growth. Parameters of growth (more extreme than or) comparable to what has been suggested from mtDNA data can be rejected for 6 out of the 10 largest data sets. When the data are separated into African and non-African samples, a constant size no-growth model can be rejected for 4 out of 8 non-African samples. Long-term growth (i.e., starting 50-100 kya) can be rejected for 2 out of 8 African samples and 5 out of 8 non-African ones. Under more complex demographic models, including a bottleneck or population subdivision, more of the data are compatible with long-term growth. One problem with the data used here is that a subset of loci may reflect the action of natural selection as well as of demography. It remains possible that the correct demographic model is one of constant population size followed by long-term growth but that at several loci the demographic signature has been obscured by balancing or diversifying selection. However, it is not clear that the data at these loci are consistent with a simple model of balancing selection; more complicated selective alternatives cannot be tested unless they are made explicit. An alternative explanation is that population size growth is more recent (e.g., upper Paleolithic) and that some of the loci have experienced recent directional selection. Given the available data, the latter hypothesis seems more likely.

Full Text

The Full Text of this article is available as a PDF (138.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Awadalla P., Eyre-Walker A., Smith J. M. Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science. 1999 Dec 24;286(5449):2524–2525. doi: 10.1126/science.286.5449.2524. [DOI] [PubMed] [Google Scholar]
  2. Bowcock A. M., Ruiz-Linares A., Tomfohrde J., Minch E., Kidd J. R., Cavalli-Sforza L. L. High resolution of human evolutionary trees with polymorphic microsatellites. Nature. 1994 Mar 31;368(6470):455–457. doi: 10.1038/368455a0. [DOI] [PubMed] [Google Scholar]
  3. Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cann R. L., Stoneking M., Wilson A. C. Mitochondrial DNA and human evolution. Nature. 1987 Jan 1;325(6099):31–36. doi: 10.1038/325031a0. [DOI] [PubMed] [Google Scholar]
  5. Cargill M., Altshuler D., Ireland J., Sklar P., Ardlie K., Patil N., Shaw N., Lane C. R., Lim E. P., Kalyanaraman N. Characterization of single-nucleotide polymorphisms in coding regions of human genes. Nat Genet. 1999 Jul;22(3):231–238. doi: 10.1038/10290. [DOI] [PubMed] [Google Scholar]
  6. Clark A. G., Weiss K. M., Nickerson D. A., Taylor S. L., Buchanan A., Stengård J., Salomaa V., Vartiainen E., Perola M., Boerwinkle E. Haplotype structure and population genetic inferences from nucleotide-sequence variation in human lipoprotein lipase. Am J Hum Genet. 1998 Aug;63(2):595–612. doi: 10.1086/301977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Di Rienzo A., Donnelly P., Toomajian C., Sisk B., Hill A., Petzl-Erler M. L., Haines G. K., Barch D. H. Heterogeneity of microsatellite mutations within and between loci, and implications for human demographic histories. Genetics. 1998 Mar;148(3):1269–1284. doi: 10.1093/genetics/148.3.1269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Di Rienzo A., Wilson A. C. Branching pattern in the evolutionary tree for human mitochondrial DNA. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1597–1601. doi: 10.1073/pnas.88.5.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fay J. C., Wu C. I. A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol Biol Evol. 1999 Jul;16(7):1003–1005. doi: 10.1093/oxfordjournals.molbev.a026175. [DOI] [PubMed] [Google Scholar]
  10. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fu Y. X. New statistical tests of neutrality for DNA samples from a population. Genetics. 1996 May;143(1):557–570. doi: 10.1093/genetics/143.1.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gonser R., Donnelly P., Nicholson G., Di Rienzo A. Microsatellite mutations and inferences about human demography. Genetics. 2000 Apr;154(4):1793–1807. doi: 10.1093/genetics/154.4.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Halushka M. K., Fan J. B., Bentley K., Hsie L., Shen N., Weder A., Cooper R., Lipshutz R., Chakravarti A. Patterns of single-nucleotide polymorphisms in candidate genes for blood-pressure homeostasis. Nat Genet. 1999 Jul;22(3):239–247. doi: 10.1038/10297. [DOI] [PubMed] [Google Scholar]
  14. Hamblin M. T., Di Rienzo A. Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am J Hum Genet. 2000 Apr 12;66(5):1669–1679. doi: 10.1086/302879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hammer M. F., Spurdle A. B., Karafet T., Bonner M. R., Wood E. T., Novelletto A., Malaspina P., Mitchell R. J., Horai S., Jenkins T. The geographic distribution of human Y chromosome variation. Genetics. 1997 Mar;145(3):787–805. doi: 10.1093/genetics/145.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harding R. M., Fullerton S. M., Griffiths R. C., Bond J., Cox M. J., Schneider J. A., Moulin D. S., Clegg J. B. Archaic African and Asian lineages in the genetic ancestry of modern humans. Am J Hum Genet. 1997 Apr;60(4):772–789. [PMC free article] [PubMed] [Google Scholar]
  17. Harpending H. C., Batzer M. A., Gurven M., Jorde L. B., Rogers A. R., Sherry S. T. Genetic traces of ancient demography. Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1961–1967. doi: 10.1073/pnas.95.4.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Harris E. E., Hey J. X chromosome evidence for ancient human histories. Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3320–3324. doi: 10.1073/pnas.96.6.3320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hawks J., Hunley K., Lee S. H., Wolpoff M. Population bottlenecks and Pleistocene human evolution. Mol Biol Evol. 2000 Jan;17(1):2–22. doi: 10.1093/oxfordjournals.molbev.a026233. [DOI] [PubMed] [Google Scholar]
  20. Hey J., Harris E. Population bottlenecks and patterns of human polymorphism. Mol Biol Evol. 1999 Oct;16(10):1423–1426. doi: 10.1093/oxfordjournals.molbev.a026054. [DOI] [PubMed] [Google Scholar]
  21. Hey J. Mitochondrial and nuclear genes present conflicting portraits of human origins. Mol Biol Evol. 1997 Feb;14(2):166–172. doi: 10.1093/oxfordjournals.molbev.a025749. [DOI] [PubMed] [Google Scholar]
  22. Hey J. The neutralist, the fly and the selectionist. Trends Ecol Evol. 1999 Jan;14(1):35–38. doi: 10.1016/s0169-5347(98)01497-9. [DOI] [PubMed] [Google Scholar]
  23. Hudson R. R., Kaplan N. L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. doi: 10.1093/genetics/111.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hudson R. R., Kaplan N. L. The coalescent process in models with selection and recombination. Genetics. 1988 Nov;120(3):831–840. doi: 10.1093/genetics/120.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jin L., Underhill P. A., Doctor V., Davis R. W., Shen P., Cavalli-Sforza L. L., Oefner P. J. Distribution of haplotypes from a chromosome 21 region distinguishes multiple prehistoric human migrations. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3796–3800. doi: 10.1073/pnas.96.7.3796. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jorde L. B., Watkins W. S., Bamshad M. J., Dixon M. E., Ricker C. E., Seielstad M. T., Batzer M. A. The distribution of human genetic diversity: a comparison of mitochondrial, autosomal, and Y-chromosome data. Am J Hum Genet. 2000 Mar;66(3):979–988. doi: 10.1086/302825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kaessmann H., Heissig F., von Haeseler A., Päbo S. DNA sequence variation in a non-coding region of low recombination on the human X chromosome. Nat Genet. 1999 May;22(1):78–81. doi: 10.1038/8785. [DOI] [PubMed] [Google Scholar]
  28. Kimmel M., Chakraborty R., King J. P., Bamshad M., Watkins W. S., Jorde L. B. Signatures of population expansion in microsatellite repeat data. Genetics. 1998 Apr;148(4):1921–1930. doi: 10.1093/genetics/148.4.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kruglyak L. Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nat Genet. 1999 Jun;22(2):139–144. doi: 10.1038/9642. [DOI] [PubMed] [Google Scholar]
  30. Nachman M. W., Bauer V. L., Crowell S. L., Aquadro C. F. DNA variability and recombination rates at X-linked loci in humans. Genetics. 1998 Nov;150(3):1133–1141. doi: 10.1093/genetics/150.3.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nachman M. W., Brown W. M., Stoneking M., Aquadro C. F. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics. 1996 Mar;142(3):953–963. doi: 10.1093/genetics/142.3.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Peterson R. J., Goldman D., Long J. C. Nucleotide sequence diversity in non-coding regions of ALDH2 as revealed by restriction enzyme and SSCP analysis. Hum Genet. 1999 Feb;104(2):177–187. doi: 10.1007/s004390050932. [DOI] [PubMed] [Google Scholar]
  33. Pritchard J. K., Seielstad M. T., Perez-Lezaun A., Feldman M. W. Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Mol Biol Evol. 1999 Dec;16(12):1791–1798. doi: 10.1093/oxfordjournals.molbev.a026091. [DOI] [PubMed] [Google Scholar]
  34. Rana B. K., Hewett-Emmett D., Jin L., Chang B. H., Sambuughin N., Lin M., Watkins S., Bamshad M., Jorde L. B., Ramsay M. High polymorphism at the human melanocortin 1 receptor locus. Genetics. 1999 Apr;151(4):1547–1557. doi: 10.1093/genetics/151.4.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Reich D. E., Goldstein D. B. Genetic evidence for a Paleolithic human population expansion in Africa. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8119–8123. doi: 10.1073/pnas.95.14.8119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Relethford J. H., Jorde L. B. Genetic evidence for larger African population size during recent human evolution. Am J Phys Anthropol. 1999 Mar;108(3):251–260. doi: 10.1002/(SICI)1096-8644(199903)108:3<251::AID-AJPA1>3.0.CO;2-H. [DOI] [PubMed] [Google Scholar]
  37. Rieder M. J., Taylor S. L., Clark A. G., Nickerson D. A. Sequence variation in the human angiotensin converting enzyme. Nat Genet. 1999 May;22(1):59–62. doi: 10.1038/8760. [DOI] [PubMed] [Google Scholar]
  38. Rogers A. R., Harpending H. Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol. 1992 May;9(3):552–569. doi: 10.1093/oxfordjournals.molbev.a040727. [DOI] [PubMed] [Google Scholar]
  39. Sherry S. T., Rogers A. R., Harpending H., Soodyall H., Jenkins T., Stoneking M. Mismatch distributions of mtDNA reveal recent human population expansions. Hum Biol. 1994 Oct;66(5):761–775. [PubMed] [Google Scholar]
  40. Slatkin M., Hudson R. R. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics. 1991 Oct;129(2):555–562. doi: 10.1093/genetics/129.2.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  42. Stiner MC, Munro ND, Surovell TA, Tchernov E, Bar-Yosef O. Paleolithic population growth pulses evidenced by small animal exploitation . Science. 1999 Jan 8;283(5399):190–194. doi: 10.1126/science.283.5399.190. [DOI] [PubMed] [Google Scholar]
  43. Stringer C. B., Andrews P. Genetic and fossil evidence for the origin of modern humans. Science. 1988 Mar 11;239(4845):1263–1268. doi: 10.1126/science.3125610. [DOI] [PubMed] [Google Scholar]
  44. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct;105(2):437–460. doi: 10.1093/genetics/105.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Takahata N. Gene identity and genetic differentiation of populations in the finite island model. Genetics. 1983 Jul;104(3):497–512. doi: 10.1093/genetics/104.3.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Templeton A. R., Clark A. G., Weiss K. M., Nickerson D. A., Boerwinkle E., Sing C. F. Recombinational and mutational hotspots within the human lipoprotein lipase gene. Am J Hum Genet. 2000 Jan;66(1):69–83. doi: 10.1086/302699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Underhill P. A., Jin L., Lin A. A., Mehdi S. Q., Jenkins T., Vollrath D., Davis R. W., Cavalli-Sforza L. L., Oefner P. J. Detection of numerous Y chromosome biallelic polymorphisms by denaturing high-performance liquid chromatography. Genome Res. 1997 Oct;7(10):996–1005. doi: 10.1101/gr.7.10.996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wall J. D. A comparison of estimators of the population recombination rate. Mol Biol Evol. 2000 Jan;17(1):156–163. doi: 10.1093/oxfordjournals.molbev.a026228. [DOI] [PubMed] [Google Scholar]
  50. Weiss K. M. On the number of members of the genus Homo who have ever lived, and some evolutionary implications. Hum Biol. 1984 Dec;56(4):637–649. [PubMed] [Google Scholar]
  51. Wise C. A., Sraml M., Easteal S. Departure from neutrality at the mitochondrial NADH dehydrogenase subunit 2 gene in humans, but not in chimpanzees. Genetics. 1998 Jan;148(1):409–421. doi: 10.1093/genetics/148.1.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Zietkiewicz E., Yotova V., Jarnik M., Korab-Laskowska M., Kidd K. K., Modiano D., Scozzari R., Stoneking M., Tishkoff S., Batzer M. Genetic structure of the ancestral population of modern humans. J Mol Evol. 1998 Aug;47(2):146–155. doi: 10.1007/pl00006371. [DOI] [PubMed] [Google Scholar]