Sex-Specific Genetic Structure and Social Organization in Central Asia: Insights from a Multi-Locus Study

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In the last two decades, mitochondrial DNA (mtDNA) and the non-recombining portion of the Y chromosome (NRY) have been extensively used in order to measure the maternally and paternally inherited genetic structure of human populations, and to infer sex-specific demography and history. Most studies converge towards the notion that among populations, women are genetically less structured than men. This has been mainly explained by a higher migration rate of women, due to patrilocality, a tendency for men to stay in their birthplace while women move to their husband's house. Yet, since population differentiation depends upon the product of the effective number of individuals within each deme and the migration rate among demes, differences in male and female effective numbers and sex-biased dispersal have confounding effects on the comparison of genetic structure as measured by uniparentally inherited markers. In this study, we develop a new multi-locus approach to analyze jointly autosomal and X-linked markers in order to aid the understanding of sex-specific contributions to population differentiation. We show that in patrilineal herder groups of Central Asia, in contrast to bilineal agriculturalists, the effective number of women is higher than that of men. We interpret this result, which could not be obtained by the analysis of mtDNA and NRY alone, as the consequence of the social organization of patrilineal populations, in which genetically related men (but not women) tend to cluster together. This study suggests that differences in sex-specific migration rates may not be the only cause of contrasting male and female differentiation in humans, and that differences in effective numbers do matter.

Vyšlo v časopise: Sex-Specific Genetic Structure and Social Organization in Central Asia: Insights from a Multi-Locus Study. PLoS Genet 4(9): e32767. doi:10.1371/journal.pgen.1000200
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000200

Souhrn

Zdroje

1. DisotellTR

1999 Human evolution: sex-specific contributions to genome variation. Curr Biol 9 R29 31

2. WilkinsJF

2006 Unraveling male and female histories from human genetic data. Curr Opin Genet Dev 16 611 617

3. SeielstadMT

MinchE

Cavalli-SforzaLL

1998 Genetic evidence for a higher female migration rate in humans. Nat Genet 20 278 280

4. SalemAH

BadrFM

GaballahMF

PääboS

1996 The genetics of traditional living: Y-chromosomal and mitochondrial lineages in the Sinai Peninsula. Am J Hum Genet 59 741 743

5. Perez-LezaunA

CalafellF

ComasD

MateuE

BoschE

1999 Sex-specific migration patterns in Central Asian populations, revealed by analysis of Y-chromosome short tandem repeats and mtDNA. Am J Hum Genet 65 208 219

6. OotaH

KitanoT

JinF

YuasaI

WangL

2002 Extreme mtDNA homogeneity in continental Asian populations. Am J Phys Anthropol 118 146 153

7. KayserM

BrauerS

WeissG

SchiefenhovelW

UnderhillP

2003 Reduced Y-chromosome, but not mitochondrial DNA, diversity in human populations from West New Guinea. Am J Hum Genet 72 281 302

8. MalyarchukB

DerenkoM

GrzybowskiT

LunkinaA

CzarnyJ

2004 Differentiation of mitochondrial DNA and Y chromosomes in Russian populations. Hum Biol 76 877 900

9. NasidzeI

LingEY

QuinqueD

DupanloupI

CordauxR

2004 Mitochondrial DNA and Y-chromosome variation in the Caucasus. Ann Hum Genet 68 205 221

10. NasidzeI

QuinqueD

OzturkM

BendukidzeN

StonekingM

2005 MtDNA and Y-chromosome variation in Kurdish groups. Ann Hum Genet 69 401 412

11. ChaixR

Quintana-MurciL

HegayT

HammerMF

MobasherZ

2007 From social to genetic structures in central Asia. Curr Biol 17 43 48

12. WilkinsJF

MarloweFW

2006 Sex-biased migration in humans: what should we expect from genetic data? Bioessays 28 290 300

13. BurtonML

MooreCC

WhitingJWM

RomneyAK

1996 Regions based on social structure. Curr Anthro 37 87 123

14. OotaH

Settheetham-IshidaW

TiwawechD

IshidaT

StonekingM

2001 Human mtDNA and Y-chromosome variation is correlated with matrilocal versus patrilocal residence. Nat Genet 29 20 21

15. Destro-BisolG

DonatiF

CoiaV

BoschiI

VerginelliF

2004 Variation of female and male lineages in sub-Saharan populations: the importance of sociocultural factors. Mol Biol Evol 21 1673 1682

16. HamiltonG

StonekingM

ExcoffierL

2005 Molecular analysis reveals tighter social regulation of immigration in patrilocal populations than in matrilocal populations. Proc Natl Acad Sci U S A 102 7476 7480

17. BolnickDA

BolnickDI

SmithDG

2006 Asymmetric male and female genetic histories among Native Americans from Eastern North America. Mol Biol Evol 23 2161 2174

18. StonekingM

1998 Women on the move. Nat Genet 20 219 220

19. WilderJA

KinganSB

MobasherZ

PilkingtonMM

HammerMF

2004 Global patterns of human mitochondrial DNA and Y-chromosome structure are not influenced by higher migration rates of females versus males. Nat Genet 36 1122 1125

20. RamachandranS

RosenbergNA

ZhivotovskyLA

FeldmanMW

2004 Robustness of the inference of human population structure: a comparison of X-chromosomal and autosomal microsatellites. Hum Genomics 1 87 97

21. KumarV

LangstiehBT

MadhaviKV

NaiduVM

SinghHP

2006 Global patterns in human mitochondrial DNA and Y-chromosome variation caused by spatial instability of the local cultural processes. PLoS Genet 2 e53

22. HammerMF

KarafetTM

ReddAJ

JarjanaziH

Santachiara-BenerecettiS

2001 Hierarchical patterns of global human Y-chromosome diversity. Mol Biol Evol 18 1189 1203

23. DupanloupI

PereiraL

BertorelleG

CalafellF

PrataMJ

2003 A recent shift from polygyny to monogamy in humans is suggested by the analysis of worldwide Y-chromosome diversity. J Mol Evol 57 85 97

24. WilderJA

MobasherZ

HammerMF

2004 Genetic evidence for unequal effective population sizes of human females and males. Mol Biol Evol 21 2047 2057

25. WilderJA

HammerMF

2007 Extraordinary population structure among the Baining of New Britain.

FriedlaenderJS

Genes, Language, and Culture History in the Southwest Pacific Oxford, UK Oxford University Press 199 207

26. SeielstadM

2000 Asymmetries in the maternal and paternal genetic histories of Colombian populations. Am J Hum Genet 67 1062 1066

27. LangergraberKE

SiedelH

MitaniJC

WranghamRW

ReynoldsV

2007 The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS ONE 2 e973

28. BazinE

GleminS

GaltierN

2006 Population size does not influence mitochondrial genetic diversity in animals. Science 312 570 572

29. HeyerE

SibertA

AusterlitzF

2005 Cultural transmission of fitness: genes take the fast lane. Trends Genet 21 234 239

30. ZerjalT

XueY

BertorelleG

WellsRS

BaoW

2003 The genetic legacy of the Mongols. Am J Hum Genet 72 717 721

31. NeelJV

1970 Lessons from a “primitive” people. Science 170 815 822

32. BlumMG

HeyerE

FrancoisO

AusterlitzF

2006 Matrilineal fertility inheritance detected in hunter-gatherer populations using the imbalance of gene genealogies. PLoS Genet 2 e122

33. HelgasonA

HrafnkelssonB

GulcherJR

WardR

StefanssonK

2003 A populationwide coalescent analysis of Icelandic matrilineal and patrilineal genealogies: evidence for a faster evolutionary rate of mtDNA lineages than Y chromosomes. Am J Hum Genet 72 1370 1388

34. WhiteDR

1988 Rethinking polygyny: co-wives, codes, and cultural systems. Curr Anthro 29 529 558

35. HeiderKG

1997 Grand valley Dani: peaceful warriors.

Case studies in cultural anthropology Forth Worth, Texas Harcourt Brace College Publishers

36. TremblayM

VezinaH

2000 New estimates of intergenerational time intervals for the calculation of age and origins of mutations. Am J Hum Genet 66 651 658

37. FennerJN

2005 Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am J Phys Anthropol 128 415 423

38. TangH

SiegmundDO

ShenP

OefnerPJ

FeldmanMW

2002 Frequentist estimation of coalescence times from nucleotide sequence data using a tree-based partition. Genetics 161 447 459

39. WhitlockMC

McCauleyDE

1999 Indirect measures of gene flow and migration: FST≠1/(4Nm+1). Heredity 82 117 125

40. BeaumontM

NicholsRA

1996 Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond 263 1619 1626

41. RoussetF

1997 Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145 1219 1228

42. PoolJE

NielsenR

2007 Population size changes reshape genomic patterns of diversity. Evolution 61 3001 3006

43. RosenbergNA

PritchardJK

WeberJL

CannHM

KiddKK

2002 Genetic structure of human populations. Science 298 2381 2385

44. ReynoldsJ

WeirBS

CockerhamCC

1983 Estimation of the Coancestry Coefficient: Basis for a Short-Term Genetic Distance. Genetics 105 767 779

45. WrightS

1939 Statistical genetics in relation to evolution. Actualités scientifiques et industrielles 802 Exposés de Biométrie et de Statistique Biologique XIII Paris Hermann et Cie

46. TamisierJC

1998 Dictionnaire des peuples. Sociétés d'Afrique, d'Amérique, d'Asie et d'Océanie Paris Larousse-Bordas

47. BalaresqueP

JoblingMA

2007 Human populations: houses for spouses. Curr Biol 17 R14 16

48. Lawson-HandleyLJ

PerrinN

2007 Advance in our understanding of mammalian sex-biased dispersal. Molecular Ecology 16 1559 1578

49. HurlesME

JoblingMA

2001 Haploid chromosomes in molecular ecology: lessons from the human Y. Mol Ecol 10 1599 1613

50. ManiatisT

FritshEF

1982 Molecular cloning. A laboratory manual New York Cold Spring Laboratory

51. ParkinEJ

KraayenbrinkT

vDGL

TsheringK

de KnijffP

2006 26-Locus Y-STR typing in a Bhutanese population sample. Forensic Science International 161 1 7

52. RosenbergNA

LiLM

WardR

PritchardJK

2003 Informativeness of genetic markers for inference of ancestry. Am J Hum Genet 73 1402 1422

53. CannHM

de TomaC

CazesL

LegrandMF

MorelV

2002 A human genome diversity cell line panel. Science 296 261 262

54. WilsonJF

GoldsteinDB

2000 Consistent long-range linkage disequilibrium generated by admixture in a Bantu-Semitic hybrid population. Am J Hum Genet 67 926 935

55. NeiM

1978 Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89 583 590

56. ExcoffierL

LavalLG

SchneiderS

2005 Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinfo Online 1 47 50

57. WeirBS

CockerhamCC

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

58. RoussetF

2008 Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 8 103 106

59. DiCiccioTJ

EfronB

1996 Bootstrap confidence intervals. Statistical Science 11 189 228

60. MantelN

1967 The detection of disease clustering and a generalized regression approach. Cancer Res 27 209 220

61. R Development Core Team 2007 R: A Language and Environment for Statistical Computing Vienna R Foundation for Statistical Computing

62. WrightS

1931 Evolution in mendelian populations. Genetics 16 97 159

63. HedrickPW

2007 Sex: differences in mutation, recombination, selection, gene flow, and genetic drift. Evolution 61 2750 2771

64. RoussetF

2004 Genetic Structure and Selection in Subdivided Populations Princeton, New Jersey Princeton University Press

65. LebloisR

EstoupA

RoussetF

2003 Influence of mutational and sampling factors on the estimation of demographic parameters in a “continuous” population under isolation by distance. Mol Biol Evol 20 491 502

66. GelmanA

CarlinJB

SternHS

RubinDB

2004 Bayesian Data Analysis. Second Edition New York Chapman & Hall/CRC

67. EstoupA

JarneP

CornuetJM

2002 Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11 1591 1604

68. DibC

FaureS

FizamesC

SamsonD

DrouotN

1996 A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 380 152 154

69. ExcoffierL

SmousePE

QuattroJM

1992 Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131 479 491

70. BeerliP

FelsensteinJ

2001 Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci U S A 98 4563 4568