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PMID: 15020430 Published · ppublish English Comparative Study Journal Article

The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations.

Genetics ·Vol. 166 ·No. 1 ·2004-01-00 ·Pages 351-72

Marth GT, Czabarka E, Murvai J, Sherry ST

Abstract

We have studied a genome-wide set of single-nucleotide polymorphism (SNP) allele frequency measures for African-American, East Asian, and European-American samples. For this analysis we derived a simple, closed mathematical formulation for the spectrum of expected allele frequencies when the sampled populations have experienced nonstationary demographic histories. The direct calculation generates the spectrum orders of magnitude faster than coalescent simulations do and allows us to generate spectra for a large number of alternative histories on a multidimensional parameter grid. Model-fitting experiments using this grid reveal significant population-specific differences among the demographic histories that best describe the observed allele frequency spectra. European and Asian spectra show a bottleneck-shaped history: a reduction of effective population size in the past followed by a recent phase of size recovery. In contrast, the African-American spectrum shows a history of moderate but uninterrupted population expansion. These differences are expected to have profound consequences for the design of medical association studies. The analytical methods developed for this study, i.e., a closed mathematical formulation for the allele frequency spectrum, correcting the ascertainment bias introduced by shallow SNP sampling, and dealing with variable sample sizes provide a general framework for the analysis of public variation data.

MeSH Terms
African Americans/genetics Alleles Americas Asia Biometry Europe Gene Frequency Genetic Variation Genetics, Population Genome, Human Humans Linkage Disequilibrium Models, Genetic Polymorphism, Single Nucleotide Population Density
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Marth Gabor T
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894, USA. [email protected]
Czabarka Eva
Murvai Janos
Sherry Stephen T
References (54)
54 references, click to expand
  1. The "hitchhiking effect" revisited.
    Genetics. 1989 Dec;123(4):887-99 PMID: 2612899
  2. Mitochondrial and nuclear genes present conflicting portraits of human origins.
    Mol Biol Evol. 1997 Feb;14(2):166-72 PMID: 9029794
  3. Population growth makes waves in the distribution of pairwise genetic differences.
    Mol Biol Evol. 1992 May;9(3):552-69 PMID: 1316531
  4. Statistical tests of neutrality of mutations.
    Genetics. 1993 Mar;133(3):693-709 PMID: 8454210
  5. Inferring coalescence times from DNA sequence data.
    Genetics. 1997 Feb;145(2):505-18 PMID: 9071603
  6. Alu evolution in human populations: using the coalescent to estimate effective population size.
    Genetics. 1997 Dec;147(4):1977-82 PMID: 9409852
  7. Heterogeneity of microsatellite mutations within and between loci, and implications for human demographic histories.
    Genetics. 1998 Mar;148(3):1269-84 PMID: 9539441
  8. Signatures of population expansion in microsatellite repeat data.
    Genetics. 1998 Apr;148(4):1921-30 PMID: 9560405
  9. Population bottlenecks and patterns of human polymorphism.
    Mol Biol Evol. 1999 Oct;16(10):1423-6 PMID: 10563023
  10. Microsatellite mutations and inferences about human demography.
    Genetics. 2000 Apr;154(4):1793-807 PMID: 10747070
  11. Human population expansion and microsatellite variation.
    Mol Biol Evol. 2000 May;17(5):757-67 PMID: 10779536
  12. Adjusting the focus on human variation.
    Trends Genet. 2000 Jul;16(7):296-302 PMID: 10858659
  13. SNP frequencies in human genes an excess of rare alleles and differing modes of selection.
    Trends Genet. 2000 Aug;16(8):335-7 PMID: 10904261
  14. When did the human population size start increasing?
    Genetics. 2000 Aug;155(4):1865-74 PMID: 10924481
  15. Estimate of the mutation rate per nucleotide in humans.
    Genetics. 2000 Sep;156(1):297-304 PMID: 10978293
  16. An SNP map of the human genome generated by reduced representation shotgun sequencing.
    Nature. 2000 Sep 28;407(6803):513-6 PMID: 11029002
  17. An SNP map of human chromosome 22.
    Nature. 2000 Sep 28;407(6803):516-20 PMID: 11029003
  18. Worldwide DNA sequence variation in a 10-kilobase noncoding region on human chromosome 22.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11354-8 PMID: 11005839
  19. Mitochondrial genome variation and the origin of modern humans.
    Nature. 2000 Dec 7;408(6813):708-13 PMID: 11130070
  20. Global patterns of human DNA sequence variation in a 10-kb region on chromosome 1.
    Mol Biol Evol. 2001 Feb;18(2):214-22 PMID: 11158380
  21. The sequence of the human genome.
    Science. 2001 Feb 16;291(5507):1304-51 PMID: 11181995
  22. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
  23. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms.
    Nature. 2001 Feb 15;409(6822):928-33 PMID: 11237013
  24. Linkage disequilibrium in the human genome.
    Nature. 2001 May 10;411(6834):199-204 PMID: 11346797
  25. Population genomics: a bridge from evolutionary history to genetic medicine.
    Hum Mol Genet. 2001 Oct 1;10(20):2199-207 PMID: 11673402
  26. Genetic perspectives on human origins and differentiation.
    Annu Rev Genomics Hum Genet. 2000;1:361-85 PMID: 11701634
  27. The signature of positive selection at randomly chosen loci.
    Genetics. 2002 Mar;160(3):1179-89 PMID: 11901132
  28. The structure of haplotype blocks in the human genome.
    Science. 2002 Jun 21;296(5576):2225-9 PMID: 12029063
  29. Searching for evidence of positive selection in the human genome using patterns of microsatellite variability.
    Mol Biol Evol. 2002 Jul;19(7):1143-53 PMID: 12082133
  30. Inferences about human demography based on multilocus analyses of noncoding sequences.
    Genetics. 2002 Jul;161(3):1209-18 PMID: 12136023
  31. Genetic analysis of African populations: human evolution and complex disease.
    Nat Rev Genet. 2002 Aug;3(8):611-21 PMID: 12154384
  32. The matrix coalescent and an application to human single-nucleotide polymorphisms.
    Genetics. 2002 Aug;161(4):1641-50 PMID: 12196407
  33. Human genome sequence variation and the influence of gene history, mutation and recombination.
    Nat Genet. 2002 Sep;32(1):135-42 PMID: 12161752
  34. Human diallelic insertion/deletion polymorphisms.
    Am J Hum Genet. 2002 Oct;71(4):854-62 PMID: 12205564
  35. Evidence for population growth in humans is confounded by fine-scale population structure.
    Trends Genet. 2002 Nov;18(11):559-63 PMID: 12414185
  36. The distribution of long range admixture linkage disequilibrium in an African-American population.
    Hum Hered. 2002;53(4):187-96 PMID: 12435883
  37. Interrogating a high-density SNP map for signatures of natural selection.
    Genome Res. 2002 Dec;12(12):1805-14 PMID: 12466284
  38. Direct estimates of human per nucleotide mutation rates at 20 loci causing Mendelian diseases.
    Hum Mutat. 2003 Jan;21(1):12-27 PMID: 12497628
  39. Sequence variations in the public human genome data reflect a bottlenecked population history.
    Proc Natl Acad Sci U S A. 2003 Jan 7;100(1):376-81 PMID: 12502794
  40. Using haplotype blocks to map human complex trait loci.
    Trends Genet. 2003 Mar;19(3):135-40 PMID: 12615007
  41. Finding genes underlying risk of complex disease by linkage disequilibrium mapping.
    Curr Opin Genet Dev. 2003 Jun;13(3):296-302 PMID: 12787793
  42. Haplotype blocks and linkage disequilibrium in the human genome.
    Nat Rev Genet. 2003 Aug;4(8):587-97 PMID: 12897771
  43. The sampling theory of selectively neutral alleles.
    Theor Popul Biol. 1972 Mar;3(1):87-112 PMID: 4667078
  44. Genetic evidence for a Paleolithic human population expansion in Africa.
    Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8119-23 PMID: 9653150
  45. The effect of selective sweeps on the variance of the allele distribution of a linked multiallele locus: hitchhiking of microsatellites.
    Theor Popul Biol. 1998 Jun;53(3):272-83 PMID: 9679322
  46. Genetic evidence for larger African population size during recent human evolution.
    Am J Phys Anthropol. 1999 Mar;108(3):251-60 PMID: 10096677
  47. Prospects for whole-genome linkage disequilibrium mapping of common disease genes.
    Nat Genet. 1999 Jun;22(2):139-44 PMID: 10369254
  48. Characterization of single-nucleotide polymorphisms in coding regions of human genes.
    Nat Genet. 1999 Jul;22(3):231-8 PMID: 10391209
  49. A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation.
    Mol Biol Evol. 1999 Jul;16(7):1003-5 PMID: 10406117
  50. Mismatch distributions of mtDNA reveal recent human population expansions.
    Hum Biol. 1994 Oct;66(5):761-75 PMID: 8001908
  51. Sampling theory for neutral alleles in a varying environment.
    Philos Trans R Soc Lond B Biol Sci. 1994 Jun 29;344(1310):403-10 PMID: 7800710
  52. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms.
    Genetics. 1995 Jun;140(2):783-96 PMID: 7498754
  53. Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling.
    Genetics. 1995 Aug;140(4):1421-30 PMID: 7498781
  54. Branching pattern in the evolutionary tree for human mitochondrial DNA.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1597-601 PMID: 2000368
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2004-01-00
Pages
351-72
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1470693
Subset
IM
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