Cited by 587Forensic and Genetic ResearchGenetic diversity and population structureGenetic Associations and Epidemiology

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Global Patterns of Linkage Disequilibrium at the CD4 Locus and Modern Human Origins

Tishkoff, S. A., Dietzsch, E., Speed, W., Pakstis, A. J., Kidd, J. R., Cheung, K., Bonné-Tamir, B., Santachiara-Benerecetti, A. S., Moral, P., Krings, M., Pääbo, S., Watson, E., Risch, N., Jenkins, T., Kidd, K. K.·1996·Science

DOI 10.1126/science.271.5254.1380

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Abstract

Haplotypes consisting of alleles at a short tandem repeat polymorphism (STRP) and an Alu deletion polymorphism at the CD4 locus on chromosome 12 were analyzed in more than 1600 individuals sampled from 42 geographically dispersed populations (13 African, 2 Middle Eastern, 7 European, 9 Asian, 3 Pacific, and 8 Amerindian). Sub-Saharan African populations had more haplotypes and exhibited more variability in frequencies of haplotypes than the Northeast African or non-African populations. The Alu deletion was nearly always associated with a single STRP allele in non-African and Northeast African populations but was associated with a wide range of STRP alleles in the sub-Saharan African populations. This global pattern of haplotype variation and linkage disequilibrium suggests a common and recent African origin for all non-African human populations.

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Short Tandem-Repeat Polymorphism/Alu Haplotype Variation at the PLAT Locus: Implications for Modern Human Origins
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“These results are consistent with those of previous studies of the PLAT Alu polymorphism in a smaller sample of populations (Perna et al. 1992; Batzer et al. 1994; Tishkoff et al. 1996b; Stoneking et al. 1997; Novick et al. 1998).”
BackgroundMethodResultInfluentialSelf-citation
Likelihood analysis of disequilibrium mapping, and related problems.
Rannala, B., & Slatkin, M. (1998) · American Journal of Human Genetics · doi:10.1086/301709 · Cited by 93
“Because Tishkoff et al. (1996) used the moments estimator for allele ages in both populations, their estimates are necessarily of t2.”
BackgroundMethodResultInfluential
An Australasian test of the recent African origin theory using the WLH-50 calvarium.
Hawks, J., Oh, S., Hunley, K., Dobson, S., Cabana, G. S., Dayalu, P., & Wolpoff, M. H. (2000) · Journal of Human Evolution · doi:10.1006/jhev.1999.0384 · Cited by 92
“4Polygenism seems to be the hypothesis a number of authors try to disprove when they address multiregional evolution (cf. Tishkoff et al., 1996; Chu et al., 1998; Cavalli-Sforza, 1998).”
Background
The role of the Y chromosome in human evolutionary studies
Hammer, M. F., & Zegura, S. L. (1996) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/(sici)1520-6505(1996)5:4 · Cited by 116
Understanding Human DNA Sequence Variation
Kídd, K. K., PAKSTIS, A. J., Speed, W. C., & Kídd, K. K. (2004) · Journal of Heredity · doi:10.1093/jhered/esh060 · Cited by 111
“This picture is seen at multiple loci in addition to those shown in Figures 6 and 7: CD4 (Tishkoff et al. 1996), DM (Tishkoff et al. 1998), COMT (DeMille et al. 2002), and RET (Chattopadhyay et al. 2003).”
MethodSelf-citation
A Diffusion Wave out of Africa
Eswaran, V. (2002) · Current Anthropology · doi:10.1086/342639 · Cited by 91
“Both patterns have been observed in present-day populations, in single-locus and in multilocus microsatellite studies (e.g., Tishkoff et al. 1996, Harpending and Eller 1999).”
Background
Genetic evidence and the modern human origins debate
Relethford, J. H. (2008) · Heredity · doi:10.1038/hdy.2008.14 · Cited by 90
“Specifically, genetic diversity outside of Africa tends to be a subset of the diversity within Africa (Tishkoff et al., 1996; Watkins et al., 2001).”
Background
Quantitative alleles of CR1: coding sequence analysis and comparison of haplotypes in two ethnic groups.
Xiang, L., Rundles, J. R., Hamilton, D., & Wilson, J. G. (1999) · Journal of Immunology · doi:10.4049/jimmunol.163.9.4939 · Cited by 90
Concerted evolution of the tandemly repeated genes encoding human U2 snRNA (the RNU2 locus) involves rapid intrachromosomal homogenization and rare interchromosomal gene conversion
Liao, D., Pavelitz, T., Kidd, J., Kidd, K., & Weiner, A. (1997) · EMBO Journal · doi:10.1093/emboj/16.3.588 · Cited by 90
Self-citation
Human evolution and the mitochondrial genome
Stoneking, M., & Soodyall, H. (1996) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(96)80028-1 · Cited by 84
HLA class I and class II DNA typing and the origin of Basques
Comas, D., Mateu, E., Calafell, F., Pérez-Lezaun, A., Bosch, E., Martínez‐Arias, R., & Bertranpetit, J. (1998) · Tissue Antigens · doi:10.1111/j.1399-0039.1998.tb02944.x · Cited by 89
An Asian–Native American paternal lineage identified by RPS4Y resequencing and by microsatellite haplotyping
Bergen, A. W., Wang, C.-Y., Tsai, J., Jefferson, K., Dey, C., Smith, K. D., Park, S.-C., Tsai, S.-J.-L., & Goldman, D. (1999) · Annals of Human Genetics · doi:10.1046/j.1469-1809.1999.6310063.x · Cited by 88
A tale of two islands: population history and mitochondrial DNA sequence variation of Bioko and São Tomé, Gulf of Guinea
Mateu, E., Comas, D., Calafell, F., Pérez-Lezaun, A., Abade, A., & Bertranpetit, J. (1997) · Annals of Human Genetics · doi:10.1046/j.1469-1809.1997.6160507.x · Cited by 88
The Extent of Linkage Disequilibrium Caused by Selection on G6PD in Humans
Saunders, M. A., Slatkin, M., Garner, C. P., Hammer, M. F., & Nachman, M. W. (2005) · Genetics · doi:10.1534/genetics.105.048140 · Cited by 107
Population Genetics of Y-Chromosome Short Tandem Repeats in Humans
Pérez-Lezaun, A., Calafell, F., Seielstad, M., Mateu, E., Comas, D., Bosch, E., & Bertranpetit, J. (1997) · Journal of Molecular Evolution · doi:10.1007/pl00006229 · Cited by 87
“Short tandem repeats in a haplotype framework can potentially answer some unresolved questions regarding the populations bearing the variation and the production and maintenance of the genetic variation (Tishkoff et al. 1996).”
Background
The human genome project and molecular anthropology.Preprint
Stoneking, M. (1997) · Genome Research · doi:10.1101/gr.7.2.87 · Cited by 86
“…reconstructing human evolution would have these same properties, and two recent studies have focused on analyzing haplotypes that consist of highly variable nuclear DNA regions that are closely linked to (Tishkoff et al. 1996) or encompass (Armour et al. 1996) more slowly evolving polymorphisms.”
Background
Correlation-Based Inference for Linkage Disequilibrium With Multiple Alleles
Zaykin, D. V., Pudovkin, A. I., & Weir, B. S. (2008) · Genetics · doi:10.1534/genetics.108.089409 · Cited by 79
“We assume multinomial sampling of haplotypes.”
Background
Extensive linkage disequilibrium in small human populations in Eurasia.
Kaessmann, H., Zöllner, S., Gustafsson, A., Wiebe, V., Laan, M., Lundeberg, J., Uhlén, M., & Pääbo, S. (2002) · American Journal of Human Genetics · doi:10.1086/339258 · Cited by 85
“Studies of LD between microsatellites (Tishkoff et al. 1996, 1998, 2000; Kidd et al. 2000) and, more recently, between SNPs (Reich et al. 2001) have provided new insights into the origin and history of human populations.”
BackgroundSelf-citation
De novo human genome assemblies reveal spectrum of alternative haplotypes in diverse populations
Wong, K. H. Y., Levy‐Sakin, M., & Kwok, P. (2018) · Nature Communications · doi:10.1038/s41467-018-05513-w · Cited by 86
Linkage Disequilibrium and Haplotype Diversity in the Genes of the Renin–Angiotensin System: Findings From the Family Blood Pressure ProgramPreprint
Zhu, X., Yan, D. L. S., Cooper, R., Luke, A., Ikeda, M. A., Chang, Y.-P. C., Weder, A. B., & Chakravarti, A. (2003) · Genome Research · doi:10.1101/gr.302003 · Cited by 78
“Our data yielded a value for FST of 0.084, with a 95% confidence interval of (0.049, 0.119) obtained by bootstrapping all sites (Weir 1996).”
MethodInfluential
DNA Sequence Variation in a 3.7-kb Noncoding Sequence 5′ of the CYP1A2 Gene: Implications for Human Population History and Natural Selection
Wooding, S., Watkins, W. S., Bamshad, M. J., Dunn, D. M., Weiss, R. B., & Jorde, L. B. (2002) · The American Journal of Human Genetics · doi:10.1086/342260 · Cited by 87
“This pattern has been observed in a number of other studies (Tishkoff et al. 1996, 2000; Calafell et al. 1997; Hammer et al. 1997; Watson et al. 1997; Alonso and Armour 2001) and agrees with a scenario in which some African populations left the continent to populate the rest of the Old World (Jorde…”
Result
Role of evolutionary history on haplotype block structure in the human genome: implications for disease mapping
Tishkoff, S. A., & Verrelli, B. C. (2003) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2003.10.010 · Cited by 83
Self-citation
Consistent Long-Range Linkage Disequilibrium Generated by Admixture in a Bantu-Semitic Hybrid Population
Wilson, J. F., & Goldstein, D. B. (2000) · The American Journal of Human Genetics · doi:10.1086/303083 · Cited by 91
“The observed patterns of LD do, however, present an important (Tishkoff et al. 1996, 1998) and largely untapped source of information regarding human evolutionary history.”
BackgroundInfluential
Nuclear DNA diversity in worldwide distributed human populations
Ziętkiewicz, E., Yotova, V., Jarník, M., Korab-Laskowska, M., Kídd, K. K., Modiano, D., Scozzari, R., Stoneking, M., Tishkoff, S. A., Batzer, M. A., et al. (1997) · Gene · doi:10.1016/s0378-1119(97)00408-3 · Cited by 88
Self-citation
SNPSTRs: Empirically Derived, Rapidly Typed, Autosomal Haplotypes for Inference of Population History and Mutational Processes
Mountain, J. L., Knight, A., Jobin, M., Gignoux, C., Miller, A., Lin, A. A., & Underhill, P. A. (2002) · Genome Research · doi:10.1101/gr.238602 · Cited by 82
“The Alu and STR originally studied by Tishkoff et al. (1996) are 9.8 kb apart, and the PLAT locus (Tishkoff et al. 2000b) spans 22 kb.”
Influential
A novel DNA sequence database for analyzing human demographic historyPreprint
Wall, J. D., Cox, M. P., Mendez, F. L., Woerner, A. E., Severson, T., & Hammer, M. F. (2008) · Genome Research · doi:10.1101/gr.075630.107 · Cited by 78
Searching for signals of evolutionary selection in 168 genes related to immune function
Walsh, E. C., Sabeti, P. C., Hutcheson, H. B., Fry, B., Schaffner, S. F., de Bakker, P. I. W., Varilly, P., Palma, A., Roy, J., Cooper, R., et al. (2005) · Human Genetics · doi:10.1007/s00439-005-0090-0 · Cited by 76
“To date, some of the strongest evidence for selection in the human genome have been identified at immunity-related loci, for example, at the HLA (Walsh et al. 2003), and loci involved in resistance to malaria (Hamblin et al. 2002; Sabeti et al. 2002; Tishkoff et al. 1996).”
Background
Fixation of the Human-Specific CMP-N-Acetylneuraminic Acid Hydroxylase Pseudogene and Implications of Haplotype Diversity for Human Evolution
Hayakawa, T., Aki, I., Varki, A. P., Satta, Y., & Takahata, N. (2005) · Genetics · doi:10.1534/genetics.105.046995 · Cited by 83
“Under this alternative, we assume that B0 arose in Africa and B2 arose somewhere in Eurasia.”
BackgroundInfluential
A reference haplotype panel for genome-wide imputation of short tandem repeats
Saini, S., Mitra, I., Mousavi, N., Feupe, S. F., & Gymrek, M. (2018) · Nature Communications · doi:10.1038/s41467-018-06694-0 · Cited by 73
Genetic studies of human diversity in East Asia
Zhang, F., Su, B., Zhang, Y., & Li, J. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2028 · Cited by 75
When Is Selection Effective?Preprint
Gravel, S. (2014) · Genetics · doi:10.1101/010934 · Cited by 78
“The reduction in diversity has been observed in human populations that have undergone strong population bottlenecks: For example, heterozygosity decreased in populations that left Africa, and further decreased with successive founder events [5, 6, 7, 8].”
Background
Foregone Conclusions?
Terrell, J. E., Kelly, K. M., & Rainbird, P. (2001) · Current Anthropology · doi:10.1086/318436 · Cited by 93
Mitochondrial evidence for the origin of hamadryas baboons.
Wildman, D., Bergman, T., Al-aghbari, A., Sterner, K., Newman, T., Phillips-Conroy, J., Jolly, C., & Disotell, T. (2004) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2003.12.014 · Cited by 76
Molecular haplotyping of genomic DNA for multiple single-nucleotide polymorphisms located kilobases apart using long-range polymerase chain reaction and intramolecular ligation
McDonald, O. G., Krynetski, E. Y., & Evans, W. E. (2002) · Pharmacogenetics · doi:10.1097/00008571-200203000-00003 · Cited by 72
“Haplotype distribution also represents the best approach to assess patterns of linkage disequilibrium, and can be used to provide insights into human evolutionary history and origin [ 14 ].”
Background
Africans and Asians abroad: genetic diversity in Europe.
Barbujani, G., & Goldstein, D. (2004) · Annual review of genomics and human genetics (Print) · doi:10.1146/annurev.genom.5.061903.180021 · Cited by 73
“They contain a broad range of haplotypes, only subsets of which, conversely, are found in the other continents (2, 68, 187), and it is in Africa that we observe the lowest levels of linkage disequilibrium (LD) worldwide (183).”
Background
The effect of single nucleotide polymorphism identification strategies on estimates of linkage disequilibrium.
Akey, J., Zhang, K., Xiong, M., & Jin, L. (2003) · Molecular biology and evolution · doi:10.1093/molbev/msg032 · Cited by 73
“Arguably, the most promising application of SNPs will be in linkage disequilibrium (LD)-based studies such as disease gene mapping (Akey, Jin, and Xiong 2001), pharmacogenetics (Wilson et al. 2001), and testing hypotheses of human evolution (Tishkoff et al. 1996).”
Background
The Concept of Self: A Study of Black Identity and Self-Esteem
Allen, R. (2001) · Contemporary Sociology A Journal of Reviews · doi:10.2307/3089410 · Cited by 73
Gene Mapping in Isolated Populations: New Roles for Old Friends?
Jorde, L. B., Watkins, W. S., Kere, J., Nyman, D., & Eriksson, A. W. (1999) · Human Heredity · doi:10.1159/000022891 · Cited by 72
Worldwide genetic analysis of the CFTR region.
Mateu, E., Calafell, F., Lao, O., Bonné-Tamir, B., Kidd, J., Pakstis, A., Kidd, K., & Bertranpetit, J. (2001) · American Journal of Human Genetics · doi:10.1086/316940 · Cited by 72
“…haplotypes with different degrees of polymorphism and with presumably different mutation rates has proved very fruitful in the understanding of different genome regions, such as CD4 (Tishkoff et al. 1996), DM (Tishkoff et al. 1998), DRD2 (Kidd et al. 1998), and the Y chromosome (Bosch et al. 1999).”
BackgroundInfluentialSelf-citation
Glacial vicariance and historical biogeography of rock ptarmigan (Lagopus mutus) in the Bering region
Holder, K., Montgomerie, R., & Friesen, V. (2000) · Molecular Ecology · doi:10.1046/j.1365-294x.2000.01005.x · Cited by 71
“For example, gradients in levels of genetic variability have been found in greenfinches (Merilä et al. 1997) and humans (Homo sapiens; Tishkoff et al. 1996), wherein haplotype diversity was highest in tropical and south temperate regions, and much lower in the formerly glaciated northern latitudes.”
Background
Genetic isolates: separate but equal?
Kruglyak, L. (1999) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.96.4.1170 · Cited by 70
Sequence Alignment with Tandem Duplication
Benson, G. (1997) · Annual International Conference on Research in Computational Molecular Biology · doi:10.1145/267521.267526 · Cited by 70
“Recently, polymorphic tandem repeats have been used to support the \Out of Africa" hypothesis of human evolution and migration [29, 1] and to suggest the evolutionary history of a microsatellite locus in primates [18].”
Understanding the accuracy of statistical haplotype inference with sequence data of known phase
Andrés, A. M., Clark, A. G., Shimmin, L., Boerwinkle, E., Sing, C. F., & Hixson, J. E. (2007) · Genetic Epidemiology · doi:10.1002/gepi.20185 · Cited by 68
“Haplotypes have thus become a common component of population genetic studies to understand mutational, recombinational, selective, and demographic dynamics of genomic regions [Tishkoff et al., 1996; Clark et al., 1998; Mateu et al., 2001; Sabeti et al., 2002; Kidd KK et al., 2004].”
BackgroundInfluential
The human Y chromosome: function, evolution and disease
Quintana‐Murci, L., Krausz, C. G., & McElreavey, K. (2001) · Forensic Science International · doi:10.1016/s0379-0738(01)00387-5 · Cited by 70
Differential Structuring of Human Populations for Homologous X and Y Microsatellite Loci
Scozzari, R., Cruciani, F., Malaspina, P., Santolamazza, P., Ciminelli, B. M., Torroni, A., Modiano, D., Wallace, D. C., Kídd, K. K., Olckers, A., et al. (1997) · The American Journal of Human Genetics · doi:10.1086/515500 · Cited by 76
“For the Y- 1994; Deka et al. 1995a, 1995b; Armour et al. 1996; linked polymorphism, all groups of populations displayed Tishkoff et al. 1996), has been used recently to infer high FST values (the correlation between random haplotypes genetic relationships among human populations.”
MethodSelf-citation
Allelic association between marker loci
Lonjou, C., Collins, A. R., & Morton, N. E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1621 · Cited by 65
DRD2 haplotypes containing the TaqI A1 allele: implications for alcoholism research.
Kidd, K., Pakstis, A., Castiglione, C., Kidd, J., Speed, W. C., Goldman, D., Knowler, W., Lu, R., & Bonné-Tamir, B. (1996) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.1996.tb01674.x · Cited by 67
Self-citation

Authors: Tishkoff, S. A., Dietzsch, E., Speed, W., Pakstis, A. J., Kidd, J. R., Cheung, K., Bonné-Tamir, B., Santachiara-Benerecetti, A. S., Moral, P., Krings, M., Pääbo, S., Watson, E., Risch, N., Jenkins, T., & Kidd, K. K.
Affiliations: Yale University (US)
University of the Witwatersrand (ZA)
B. Bonné-Tamir is in the Department of Human Genetics, Sackler Faculty of Medicine, Tel Aviv University, 69978 Ramat Aviv, Israel.
A. S. Santachiara-Benerecetti is in the Buzzati Traverso Department of Genetics and Microbiology, University of Pavia, Via Abbiategrasso 207, 27100 Pavia, Italy.
Universitat de Barcelona (ES)
Ludwig-Maximilians-Universität München (DE)
Massey University (NZ)
Stanford Medicine (US)
S. A. Tishkoff, W. Speed, A. J. Pakstis, J. R. Kidd, K. Cheung, and K. K. Kidd are in the Department of Genetics, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520-8005, USA.
ORCID: Tishkoff, S. A.
Pakstis, A. J.
Moral, P.
Pääbo, S.
Risch, N.
Jenkins, T.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 1996-03-08
Volume: 271
Issue: 5254
Pages: 1380-1387
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.271.5254.1380
OpenAlex: W1971604012
Cited by: 587
References: 64
Citations by year: 2026: 2 · 2025: 5 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 9 · 2020: 5 · 2019: 1 · 2018: 8 · 2017: 6 · 2016: 5 · 2015: 9 · 2014: 12 · 2013: 10 · 2012: 14
FWCI: 27.44
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: National Institutes of Health (5r01hg000348-09)
National Institute on Alcohol Abuse and Alcoholism (R01AA009379, AA09379)
National Institute of Mental Health (MH39 239)
National Human Genome Research Institute (HG00348)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Keywords: linkage disequilibrium, chromosome 12, short tandem repeat polymorphism, haplotype variation, human origins, African origin of modern humans, sub-Saharan African populations, population genetics
MeSH terms: Africa, Alleles, Animals, Base Sequence, Chromosomes, Human, Pair 12, Gene Frequency, Haplotypes, Humans, Molecular Sequence Data, Polymorphism, Genetic, Primates, Repetitive Sequences, Nucleic Acid, Genetic Variation, Hominidae, CD4 Antigens, Linkage Disequilibrium, Sequence Deletion, Evolution, Molecular

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Global Patterns of Linkage Disequilibrium at the CD4 Locus and Modern Human Origins

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