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Cited by 498Forensic and Genetic ResearchGenetic diversity and population structurePleistocene-Era Hominins and Archaeology

The DOI matches its Crossref record; 49 of the 50 references it cites were found in a registry or an index; none of the 18 sources its claims cite is checked for support yet.

A recent bottleneck of Y chromosome diversity coincides with a global change in culture

Open access
Karmin, Monika, Saag, Lauri, Vicente, Mário, Sayres, Melissa A. Wilson, Järve, Mari, Talas, Ulvi Gerst, Rootsi, Siiri, Ilumäe, Anne-Mai, Mägi, Reedik, Mitt, Mario, Pagani, Luca, Puurand, Tarmo, Faltyskova, Zuzana, Clemente, Florian, Cardona, Alexia, Metspalu, Ene, Sahakyan, Hovhannes, Yunusbayev, Bayazit, Hudjashov, Georgi, DeGiorgio, Michael, Loogväli, Eva-Liis, Eichstaedt, Christina, Eelmets, Mikk, Chaubey, Gyaneshwer, Tambets, Kristiina, Litvinov, Sergei, Mormina, Maru, Xue, Yali, Ayub, Qasim, Zoraqi, Grigor, Korneliussen, Thorfinn Sand, Akhatova, Farida, Lachance, Joseph, Tishkoff, Sarah, Momynaliev, Kuvat, Ricaut, François-Xavier, Kusuma, Pradiptajati, Razafindrazaka, Harilanto, Pierron, Denis, Cox, Murray P., Sultana, Gazi Nurun Nahar, Willerslev, Rane, Muller, Craig, Westaway, Michael, Lambert, David, Skaro, Vedrana, Kovačevic´, Lejla, Turdikulova, Shahlo, Dalimova, Dilbar, Khusainova, Rita, Trofimova, Natalya, Akhmetova, Vita, Khidiyatova, Irina, Lichman, Daria V., Isakova, Jainagul, Pocheshkhova, Elvira, Sabitov, Zhaxylyk, Barashkov, Nikolay A., Nymadawa, Pagbajabyn, Mihailov, Evelin, Seng, Joseph Wee Tien, Evseeva, Irina, Migliano, Andrea Bamberg, Abdullah, Syafiq, Andriadze, George, Primorac, Dragan, Atramentova, Lubov, Utevska, Olga, Yepiskoposyan, Levon, Marjanovic´, Damir, Kushniarevich, Alena, Behar, Doron M., Gilissen, Christian, Vissers, Lisenka, Veltman, Joris A., Balanovska, Elena, Derenko, Miroslava, Malyarchuk, Boris, Metspalu, Andres, Fedorova, Sardana, Eriksson, Anders, Manica, Andrea, Mendez, Fernando L., Karafet, Tatiana M., Veeramah, Krishna R., Bradman, Neil, Hammer, Michael F., Osipova, Ludmila P., Balanovsky, Oleg, Khusnutdinova, Elza K., Johnsen, Knut, Remm, Maido, Thomas, Mark G., Tyler-Smith, Chris, Underhill, Peter A., Willerslev, Eske, Nielsen, Rasmus, Metspalu, Mait, Villems, Richard, Kivisild, Toomas·2015·Genome Research

Abstract

It is commonly thought that human genetic diversity in non-African populations was shaped primarily by an out-of-Africa dispersal 50–100 thousand yr ago (kya). Here, we present a study of 456 geographically diverse high-coverage Y chromosome sequences, including 299 newly reported samples. Applying ancient DNA calibration, we date the Y-chromosomal most recent common ancestor (MRCA) in Africa at 254 (95% CI 192–307) kya and detect a cluster of major non-African founder haplogroups in a narrow time interval at 47–52 kya, consistent with a rapid initial colonization model of Eurasia and Oceania after the out-of-Africa bottleneck. In contrast to demographic reconstructions based on mtDNA, we infer a second strong bottleneck in Y-chromosome lineages dating to the last 10 ky. We hypothesize that this bottleneck is caused by cultural changes affecting variance of reproductive success among males.

Overview

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TL;DR

This study analyzes 456 high-coverage Y chromosome sequences, including 299 newly reported samples, to reconstruct global Y chromosome diversity and demography. It dates the Y-chromosomal MRCA in Africa at 254 kya, finds a narrow non-African founder haplogroup cluster at 47–52 kya, and infers a second strong Y-chromosome bottleneck in the last 10 ky that may reflect culturally driven changes in male reproductive success.

Key findings

  • From 456 geographically diverse high-coverage Y chromosome sequences, the authors retained 8.8 Mb per individual and 35,700 SNPs with >95% call rate; they estimated the Y binary SNP mutation rate at 0.74 × 10−9 per bp per yr (95% CI 0.63–0.95 × 10−9).
  • The Y-chromosomal MRCA in Africa was dated to 254 kya (95% CI 192–307 kya); African and non-African lineages separated at 68–72 kya (95% CI 52–87 kya), followed by a narrow interval at 47–52 kya (95% CI 36–62 kya) when major non-African founder haplogroups differentiated.
  • Bayesian skyline plots of 320 Y chromosomes and mtDNA from the same individuals both showed increases in effective population size at ∼40–60 kya, but mtDNA Ne estimates were consistently more than twice as high as Y chromosome estimates; the Y plot suggested a reduction around 8–4 kya, when female Ne was up to 17-fold higher than male Ne.
  • Many Eurasian Y haplogroups coalesced within the last 15 ky, with novel region-specific clades coalescing within the last 4–8 ky; regional pairwise divergence times also clustered around peopling of the Americas at ∼15 kya.

Methods

  • The study combined 299 new unrelated male samples from 110 populations with publicly available data for 456 total sequences; two Mbo individuals of haplogroup A00 were sequenced to root the phylogeny, and quality checks included Estonian first-degree relatives, Dutch father-son pairs, and duplicate samples.
  • Whole-genome sequencing used Complete Genomics at >40× coverage for blood and >80× for saliva, with Illumina HiSeq 2000 at 30× aimed coverage for the A00 samples; after filtering, analyses used 8.8 Mb of reliable Chr Y sequence and 35,700 high-quality biallelic SNPs.
  • Coalescent times and phylogenies were estimated with BEAST v1.8.0, summary statistics with Arlequin v3.5.1.3, and demographic scenarios with FastSimCoal2 simulations; the mutation rate was calibrated using ancient DNA from the 12.6-ky-old Anzick (Q1b) and 4-ky-old Saqqaq (Q2b) specimens.

Limitations

  • The paper states that the mutation rate estimate is based on only two ancient DNA samples from a relatively recent time horizon and the same Y chromosome haplogroup, though it notes an independent estimate of 0.76 × 10−9 per bp per yr from a different, older ancient DNA specimen.
  • The authors note that cross-species mapping showed 4.6% discordance at positions separating A2′5 and BT, higher than the 1%–2% predicted from human-chimpanzee divergence, likely reflecting mapping uncertainties.
  • The paper states that because the Y chromosome is essentially a single locus with very low Ne, the results cannot refute alternative models of earlier Middle Pleistocene dispersals (100–130 kya) from Africa; such evidence could be embedded only in the autosomal genome.
  • The authors state that population structure combined with unbalanced sampling can lead Bayesian skyline plots to infer false population declines, and that most existing methods are underpowered to detect Ne changes within the past few thousand years from recombining genome-wide data.
  • The cultural explanation for the male-specific bottleneck is presented as a hypothesis; the paper notes that the inferred mid-Holocene Ne dips may also represent a genuine population collapse following the introduction of farming.

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Registry

Crossref · 10.1101/gr.186684.114

Cites

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Statistics

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Figures

Figure 1. The phylogenetic tree of 456 whole Y chromosome sequences and a map of sampling locations. The phylogenetic tree is reconstructed using BEAST. Clades coalescing within 10% of the overall depth of the tree have been collapsed. Only main haplogroup labels are shown (details are provided in Supplemental Information 6). Colors indicate geographic origin of samples (Supplemental Table S1), and fill proportions of the collapsed clades represent the proportion of samples from a given region. Asterisk (*) marks the inclusion of samples from Caucasus area. Personal Genomes Project (http://www.personalgenomes.org) samples of unknown and mixed geographic/ethnic origin are shown in black. The proposed structure of Y chromosome haplogroup naming (Supplemental Table S5) is given in Roman numbers on the y-axis.
Figure 1. The phylogenetic tree of 456 whole Y chromosome sequences and a map of sampling locations. The phylogenetic tree is reconstructed using BEAST. Clades coalescing within 10% of the overall depth of the tree have been collapsed. Only main haplogroup labels are shown (details are provided in Supplemental Information 6). Colors indicate geographic origin of samples (Supplemental Table S1), and fill proportions of the collapsed clades represent the proportion of samples from a given region. Asterisk (*) marks the inclusion of samples from Caucasus area. Personal Genomes Project (http://www.personalgenomes.org) samples of unknown and mixed geographic/ethnic origin are shown in black. The proposed structure of Y chromosome haplogroup naming (Supplemental Table S5) is given in Roman numbers on the y-axis.CC BY-NC · PubMed Central
Figure 2. Cumulative Bayesian skyline plots of Y chromosome and mtDNA diversity by world regions. The red dashed lines highlight the horizons of 10 kya and 50 kya. Individual plots for each region are presented in Supplemental Figure S4A.
Figure 2. Cumulative Bayesian skyline plots of Y chromosome and mtDNA diversity by world regions. The red dashed lines highlight the horizons of 10 kya and 50 kya. Individual plots for each region are presented in Supplemental Figure S4A.CC BY-NC · PubMed Central

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Citations

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Research works printed but not linked: 1

  1. Fuller D . 2003. An agricultural perspective on Dravidian historical linguistics: archaeological crop packages, livestock and Dravidian crop vocabulary. In Examining the farming/language dispersal hypothesis (ed. Bellwood P , Renfrew C ), pp. 191–213. The McDonald Institute for Archaeological Research, Cambridge, UK.

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Metadata

Authors
Karmin, M., Saag, L., Vicente, M., Sayres, M. A. W., Järve, M., Talas, U. G., Rootsi, S., Ilumäe, A.-M., Mägi, R., Mitt, M., Pagani, L., Puurand, T., Faltyskova, Z., Clemente, F., Cardona, A., Metspalu, E., Sahakyan, H., Yunusbayev, B., Hudjashov, G., DeGiorgio, M., Loogväli, E.-L., Eichstaedt, C., Eelmets, M., Chaubey, G., Tambets, K., Litvinov, S., Mormina, M., Xue, Y., Ayub, Q., Zoraqi, G., Korneliussen, T. S., Akhatova, F., Lachance, J., Tishkoff, S., Momynaliev, K., Ricaut, F.-X., Kusuma, P., Razafindrazaka, H., Pierron, D., Cox, M. P., Sultana, G. N. N., Willerslev, R., Muller, C., Westaway, M., Lambert, D., Skaro, V., Kovačevic´, L., Turdikulova, S., Dalimova, D., Khusainova, R., Trofimova, N., Akhmetova, V., Khidiyatova, I., Lichman, D. V., Isakova, J., Pocheshkhova, E., Sabitov, Z., Barashkov, N. A., Nymadawa, P., Mihailov, E., Seng, J. W. T., Evseeva, I., Migliano, A. B., Abdullah, S., Andriadze, G., Primorac, D., Atramentova, L., Utevska, O., Yepiskoposyan, L., Marjanovic´, D., Kushniarevich, A., Behar, D. M., Gilissen, C., Vissers, L., Veltman, J. A., Balanovska, E., Derenko, M., Malyarchuk, B., Metspalu, A., Fedorova, S., Eriksson, A., Manica, A., Mendez, F. L., Karafet, T. M., Veeramah, K. R., Bradman, N., Hammer, M. F., Osipova, L. P., Balanovsky, O., Khusnutdinova, E. K., Johnsen, K., Remm, M., Thomas, M. G., Tyler-Smith, C., Underhill, P. A., Willerslev, E., Nielsen, R., Metspalu, M., Villems, R., & Kivisild, T.
Affiliations
  • Estonian Biocentre (EE)
  • University of Cambridge (GB)
  • University of California, Berkeley (US)
  • University of Tartu (EE)
  • Institute of Molecular Biology (AM)
  • Russian Academy of Sciences (RU)
  • University of Auckland (NZ)
  • Pennsylvania State University (US)
  • University of Winchester (GB)
  • Wellcome Sanger Institute (GB)
  • University of Medicine Tirana (AL)
  • University of Copenhagen (DK)
  • Bashkir State University (RU)
  • Georgia Institute of Technology (US)
  • University of Pennsylvania (US)
  • Centre National de la Recherche Scientifique (FR)
  • Massey University (NZ)
  • University of Dhaka (BD)
  • Aarhus University (DK)
  • Griffith University (AU)
  • Academy of Sciences Republic of Uzbekistan (UZ)
  • Institute of Cytology and Genetics (RU)
  • National Academy of Sciences of the Republic of Kyrgyzstan (KG)
  • Kuban State Medical University (RU)
  • L. N. Gumilyov Eurasian National University (KZ)
  • National Cancer Centre Singapore (SG)
  • Anthony Nolan (GB)
  • University College London (GB)
  • Raja Isteri Pengiran Anak Saleha Hospital (BN)
  • V. N. Karazin Kharkiv National University (UA)
  • National Academy of Sciences of Belarus (BY)
  • Radboud University Medical Center (NL)
  • North-Eastern Federal University (RU)
  • Stanford Medicine (US)
  • University of Arizona (US)
  • Stony Brook University (US)
  • University Hospital of North Norway (NO)
  • Estonian Academy of Sciences (EE)
Corresponding author
  • Karmin, Monika
  • Kivisild, Toomas
Venue
Genome Research
Published
2015-03-13
Volume
25
Issue
4
Pages
459-466
ISSN
  • 1088-9051 (ISSN-L)
  • 1549-5469
OpenAlex
W7014680338
Cited by
485
References
50
Citations by year
2026: 30 · 2025: 34 · 2024: 45 · 2023: 32 · 2022: 28 · 2021: 89 · 2020: 46 · 2019: 40 · 2018: 40 · 2017: 56 · 2016: 34 · 2015: 11
Type
posted content
Language
en
Open access
Locations
  • Genome Research (publishedVersion)
  • PubMed (publishedVersion)
  • Oxford University Research Archive (ORA) (University of Oxford) (publishedVersion)
  • PubMed Central (publishedVersion, cc-by-nc)
  • Winchester Research Repository (submittedVersion)
  • Griffith Research Online (submittedVersion, cc-by-nc)
  • Nazarbayev University Repository (Nazarbayev University) (submittedVersion)
  • Arizona State University Library Digital Repository (Arizona State University) (submittedVersion, cc-by-nc-nd)
  • HAL (submittedVersion, other-oa)
  • UCL Discovery (University College London) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc)
  • zvestiya of the National Academy of Sciences of Belarus (National Academy of Sciences of Belarus) (submittedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
  • King Abdullah University of Science and Technology Repository (King Abdullah University of Science and Technology) (submittedVersion, cc-by-nc)
  • Radboud Repository (Radboud University) (submittedVersion)
  • Padua Research Archive (University of Padova) (submittedVersion, cc-by-nc)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
Funders
  • Estonian and European Research (infrastructure) Roadmap (3.2.0304.11-0312)
  • Estonian Biocentre and Estonian Institutional Research (IUT24-1)
  • Estonian Science Foundation (8973)
  • Estonian Research Council (PUT766)
  • Russian Federation President (MK-2845.2014.4)
  • ERC Starting Investigator (FP7-261213)
  • Estonian Centre of Excellence in Genomics (3.2.0101.08-0011)
  • Estonian Ministry of Education and Research (SF0180026s09)
  • Centre of Translational Genomics of the University of Tartu (SP1GVARENG)
  • Russian Foundation for Basic Research (14-04-00725-a)
  • Russian Humanitarian Scientific Foundation (13-11-02014)
  • Presidium of Russian Academy of Sciences (12-I-P30-12)
  • Russian Science Foundation (14-14-00827)
  • Wellcome Trust (098051)
  • Leverhulme Program (RP2011-R-045)
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
  • Social Sciences › Anthropology › Pleistocene-Era Hominins and Archaeology
Keywords
Y chromosome, human genetic variation, dispersal out of Africa, population bottleneck, Y-chromosome lineages, reproductive success, cultural change
MeSH terms
Base Sequence, DNA, Mitochondrial, Genetics, Population, Haplotypes, Humans, Male, Models, Genetic, Phylogeny, Genetic Variation, Sequence Analysis, DNA, Evolution, Molecular, Chromosomes, Human, Y, Racial Groups

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