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Human Population Differentiation Is Strongly Correlated with Local Recombination Rate


Allele frequency differences across populations can provide valuable information both for studying population structure and for identifying loci that have been targets of natural selection. Here, we examine the relationship between recombination rate and population differentiation in humans by analyzing two uniformly-ascertained, whole-genome data sets. We find that population differentiation as assessed by inter-continental FST shows negative correlation with recombination rate, with FST reduced by 10% in the tenth of the genome with the highest recombination rate compared with the tenth of the genome with the lowest recombination rate (P≪10−12). This pattern cannot be explained by the mutagenic properties of recombination and instead must reflect the impact of selection in the last 100,000 years since human continental populations split. The correlation between recombination rate and FST has a qualitatively different relationship for FST between African and non-African populations and for FST between European and East Asian populations, suggesting varying levels or types of selection in different epochs of human history.


Vyšlo v časopise: Human Population Differentiation Is Strongly Correlated with Local Recombination Rate. PLoS Genet 6(3): e32767. doi:10.1371/journal.pgen.1000886
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000886

Souhrn

Allele frequency differences across populations can provide valuable information both for studying population structure and for identifying loci that have been targets of natural selection. Here, we examine the relationship between recombination rate and population differentiation in humans by analyzing two uniformly-ascertained, whole-genome data sets. We find that population differentiation as assessed by inter-continental FST shows negative correlation with recombination rate, with FST reduced by 10% in the tenth of the genome with the highest recombination rate compared with the tenth of the genome with the lowest recombination rate (P≪10−12). This pattern cannot be explained by the mutagenic properties of recombination and instead must reflect the impact of selection in the last 100,000 years since human continental populations split. The correlation between recombination rate and FST has a qualitatively different relationship for FST between African and non-African populations and for FST between European and East Asian populations, suggesting varying levels or types of selection in different epochs of human history.


Zdroje

1. WeirBS

CockerhamCC

1984 Estimating F-statistics for the analysis of population structure. Evolution 38 1358 1370

2. WrightS

1943 Isolation by Distance. Genetics 28 114 138

3. JakobssonM

ScholzSW

ScheetP

GibbsJR

VanLiereJM

2008 Genotype, haplotype and copy-number variation in worldwide human populations. Nature 451 998 1003

4. KeinanA

MullikinJC

PattersonN

ReichD

2007 Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nat Genet 39 1251 1255

5. KeinanA

MullikinJC

PattersonN

ReichD

2009 Accelerated genetic drift on chromosome X during the human dispersal out of Africa. Nat Genet 41 66 70

6. LewontinRC

1972 The apportionment of human diversity.

DobzhanskyT

HechtMK

SteereWC

Evolutionary Biology 6 New York Appleton-Century-Crofts 381 398

7. LiJZ

AbsherDM

TangH

SouthwickAM

CastoAM

2008 Worldwide human relationships inferred from genome-wide patterns of variation. Science 319 1100 1104

8. The International HapMap Consortium 2005 A haplotype map of the human genome. Nature 437 1299 1320

9. The International HapMap Consortium 2007 A second generation human haplotype map of over 3.1 million SNPs. Nature 449 851 861

10. WallJD

CoxMP

MendezFL

WoernerA

SeversonT

2008 A novel DNA sequence database for analyzing human demographic history. Genome Res 18 1354 1361

11. AkeyJM

ZhangG

ZhangK

JinL

ShriverMD

2002 Interrogating a high-density SNP map for signatures of natural selection. Genome Res 12 1805 1814

12. NielsenR

HellmannI

HubiszM

BustamanteC

ClarkAG

2007 Recent and ongoing selection in the human genome. Nat Rev Genet 8 857 868

13. SabetiPC

VarillyP

FryB

LohmuellerJ

HostetterE

2007 Genome-wide detection and characterization of positive selection in human populations. Nature 449 913 918

14. WeirBS

CardonLR

AndersonAD

NielsenDM

HillWG

2005 Measures of human population structure show heterogeneity among genomic regions. Genome Res 15 1468 1476

15. ChenH

PattersonN

ReichDE

2010 Population differentiation as a test for selective sweeps. Genome Res

16. BarreiroLB

LavalG

QuachH

PatinE

Quintana-MurciL

2008 Natural selection has driven population differentiation in modern humans. Nat Genet 40 340 345

17. KulathinalRJ

BennettSM

FitzpatrickCL

NoorMA

2008 Fine-scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. Proc Natl Acad Sci U S A 105 10051 10056

18. BegunDJ

AquadroCF

1992 Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356 519 520

19. BegunDJ

HollowayAK

StevensK

HillierLW

PohYP

2007 Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5 e310 doi:10.1371/journal.pbio.0050310

20. HellmannI

MangY

GuZ

LiP

de la VegaFM

2008 Population genetic analysis of shotgun assemblies of genomic sequences from multiple individuals. Genome Res 18 1020 1029

21. NachmanMW

2001 Single nucleotide polymorphisms and recombination rate in humans. Trends Genet 17 481 485

22. CaiJJ

MacphersonJM

SellaG

PetrovDA

2009 Pervasive hitchhiking at coding and regulatory sites in humans. PLoS Genet 5 e1000336 doi:10.1371/journal.pgen.1000336

23. NachmanMW

BauerVL

CrowellSL

AquadroCF

1998 DNA variability and recombination rates at X-linked loci in humans. Genetics 150 1133 1141

24. HammerMF

GarriganD

WoodE

WilderJA

MobasherZ

2004 Heterogeneous patterns of variation among multiple human x-linked Loci: the possible role of diversity-reducing selection in non-Africans. Genetics 167 1841 1853

25. SpencerCC

DeloukasP

HuntS

MullikinJ

MyersS

2006 The influence of recombination on human genetic diversity. PLoS Genet 2 e148 doi:10.1371/journal.pgen.0020148

26. WrightSI

FoxeJP

DeRose-WilsonL

KawabeA

LooseleyM

2006 Testing for effects of recombination rate on nucleotide diversity in natural populations of Arabidopsis lyrata. Genetics 174 1421 1430

27. HellmannI

EbersbergerI

PtakSE

PaaboS

PrzeworskiM

2003 A neutral explanation for the correlation of diversity with recombination rates in humans. Am J Hum Genet 72 1527 1535

28. HellmannI

PruferK

JiH

ZodyMC

PaaboS

2005 Why do human diversity levels vary at a megabase scale? Genome Res 15 1222 1231

29. TenaillonMI

U'RenJ

TenaillonO

GautBS

2004 Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21 1214 1225

30. StephanW

MitchellSJ

1992 Reduced levels of DNA polymorphism and fixed between-population differences in the centromeric region of Drosophila ananassae. Genetics 132 1039 1045

31. SmithJM

HaighJ

1974 The hitch-hiking effect of a favourable gene. Genet Res 23 23 35

32. CharlesworthB

MorganMT

CharlesworthD

1993 The effect of deleterious mutations on neutral molecular variation. Genetics 134 1289 1303

33. KauerM

ZangerlB

DieringerD

SchlottererC

2002 Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations of Drosophila melanogaster. Genetics 160 247 256

34. WallJD

AndolfattoP

PrzeworskiM

2002 Testing models of selection and demography in Drosophila simulans. Genetics 162 203 216

35. FayJC

WuCI

2000 Hitchhiking under positive Darwinian selection. Genetics 155 1405 1413

36. LercherMJ

HurstLD

2002 Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet 18 337 340

37. MagniGE

Von BorstelRC

1962 Different Rates of Spontaneous Mutation during Mitosis and Meiosis in Yeast. Genetics 47 1097 1108

38. StrathernJN

ShaferBK

McGillCB

1995 DNA synthesis errors associated with double-strand-break repair. Genetics 140 965 972

39. McVickerG

GordonD

DavisC

GreenP

2009 Widespread genomic signatures of natural selection in hominid evolution. PLoS Genet 5 e1000471 doi:10.1371/journal.pgen.1000471

40. NielsenR

2005 Molecular signatures of natural selection. Annu Rev Genet 39 197 218

41. CharlesworthB

NordborgM

CharlesworthD

1997 The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res 70 155 174

42. BegunDJ

AquadroCF

1993 African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365 548 550

43. StephanW

XingL

KirbyDA

BravermanJM

1998 A test of the background selection hypothesis based on nucleotide data from Drosophila ananassae. Proc Natl Acad Sci U S A 95 5649 5654

44. CharlesworthB

CoyneJA

BartonNH

1987 The relative rates of evolution of sex chromosomes and autosomes. The American Naturalist 130 113 146

45. CharlesworthB

1998 Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol 15 538 543

46. HindsDA

StuveLL

NilsenGB

HalperinE

EskinE

2005 Whole-genome patterns of common DNA variation in three human populations. Science 307 1072 1079

47. PatilN

BernoAJ

HindsDA

BarrettWA

DoshiJM

2001 Blocks of limited haplotype diversity revealed by high-resolution scanning of human chromosome 21. Science 294 1719 1723

48. KongA

GudbjartssonDF

SainzJ

JonsdottirGM

GudjonssonSA

2002 A high-resolution recombination map of the human genome. Nat Genet 31 241 247

49. LahiriSN

2003 Resampling methods for dependent data. New York Springer

50. KunschHR

1989 The jackknife and the bootstrap for general stationary observations. The Annals of Statistics 17 1217 1241

51. LiuRY

SinghK

1992 Moving blocks jackknife and bootstrap capture weak dependence.

LePageR

BillardL

Exploring the limits of bootstrap New York John Wiley 225 248

52. GajerP

SchatzM

SalzbergSL

2004 Automated correction of genome sequence errors. Nucleic Acids Res 32 562 569

53. CharlesworthB

1996 Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet Res 68 131 149

54. LohmuellerKE

IndapAR

SchmidtS

BoykoAR

HernandezRD

2008 Proportionally more deleterious genetic variation in European than in African populations. Nature 451 994 997

55. ChenY

MarshBJ

StephanW

2000 Joint effects of natural selection and recombination on gene flow between Drosophila ananassae populations. Genetics 155 1185 1194

56. SantiagoE

CaballeroA

2005 Variation after a selective sweep in a subdivided population. Genetics 169 475 483

57. The International HapMap 3 Consortium 2010 An integrated haplotype map of rare and common genetic variation in diverse human populations. In revision

58. KaiserJ

2008 DNA sequencing. A plan to capture human diversity in 1000 genomes. Science 319 395

59. FrisseL

HudsonRR

BartoszewiczA

WallJD

DonfackJ

2001 Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet 69 831 843

60. PluzhnikovA

Di RienzoA

HudsonRR

2002 Inferences about human demography based on multilocus analyses of noncoding sequences. Genetics 161 1209 1218

61. VoightBF

AdamsAM

FrisseLA

QianY

HudsonRR

2005 Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci U S A 102 18508 18513

62. StumpfMP

McVeanGA

2003 Estimating recombination rates from population-genetic data. Nat Rev Genet 4 959 968

63. LiN

StephensM

2003 Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165 2213 2233

64. FearnheadP

HardingRM

SchneiderJA

MyersS

DonnellyP

2004 Application of coalescent methods to reveal fine-scale rate variation and recombination hotspots. Genetics 167 2067 2081

65. McVeanGA

MyersSR

HuntS

DeloukasP

BentleyDR

2004 The fine-scale structure of recombination rate variation in the human genome. Science 304 581 584

66. O'ReillyPF

BirneyE

BaldingDJ

2008 Confounding between recombination and selection, and the Ped/Pop method for detecting selection. Genome Res 18 1304 1313

67. ReedFA

TishkoffSA

2006 Positive selection can create false hotspots of recombination. Genetics 172 2011 2014

68. MyersS

BottoloL

FreemanC

McVeanG

DonnellyP

2005 A fine-scale map of recombination rates and hotspots across the human genome. Science 310 321 324

69. HsuF

KentWJ

ClawsonH

KuhnRM

DiekhansM

2006 The UCSC Known Genes. Bioinformatics 22 1036 1046

70. ReichD

ThangarajK

PattersonN

PriceAL

SinghL

2009 Reconstructing Indian population history. Nature 461 489 494

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