The selection landscape and genetic legacy of ancient Eurasians.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
received:
17
09
2022
accepted:
03
10
2023
medline:
11
1
2024
pubmed:
11
1
2024
entrez:
10
1
2024
Statut:
ppublish
Résumé
The Holocene (beginning around 12,000 years ago) encompassed some of the most significant changes in human evolution, with far-reaching consequences for the dietary, physical and mental health of present-day populations. Using a dataset of more than 1,600 imputed ancient genomes
Identifiants
pubmed: 38200293
doi: 10.1038/s41586-023-06705-1
pii: 10.1038/s41586-023-06705-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
312-320Informations de copyright
© 2024. The Author(s).
Références
Allentoft, M. E. et al. Population genomics of post-glacial western Eurasia. Nature https://doi.org/10.1038/s41586-023-06865-0 (2024).
Page, A. E. et al. Reproductive trade-offs in extant hunter-gatherers suggest adaptive mechanism for the Neolithic expansion. Proc. Natl Acad. Sci. USA 113, 4694–4699 (2016).
pubmed: 27071109
pmcid: 4855554
doi: 10.1073/pnas.1524031113
Marciniak, S., Bergey, C., Silva, A. M. & Hałuszko, A. An integrative skeletal and paleogenomic analysis of prehistoric stature variation suggests relatively reduced health for early European farmers. Proc. Natl Acad. Sci. USA 119, e2106743119 (2022).
Visscher, P. M. et al. 10 years of GWAS discovery: biology, function and translation. Am. J. Hum. Genet. 101, 5–22 (2017).
pubmed: 28686856
pmcid: 5501872
doi: 10.1016/j.ajhg.2017.06.005
Bycroft, C. et al. The UK Biobank resource with deep phenotyping and genomic data. Nature 562, 203–209 (2018).
pubmed: 30305743
pmcid: 6786975
doi: 10.1038/s41586-018-0579-z
Vitti, J. J., Grossman, S. R. & Sabeti, P. C. Detecting natural selection in genomic data. Annu. Rev. Genet. 47, 97–120 (2013).
pubmed: 24274750
doi: 10.1146/annurev-genet-111212-133526
Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015).
pubmed: 26595274
pmcid: 4918750
doi: 10.1038/nature16152
Ju, D. & Mathieson, I. The evolution of skin pigmentation-associated variation in West Eurasia. Proc. Natl Acad. Sci. USA 118, e2009227118 (2021).
pubmed: 33443182
doi: 10.1073/pnas.2009227118
Wilde, S. et al. Direct evidence for positive selection of skin, hair and eye pigmentation in Europeans during the last 5,000 y. Proc. Natl Acad. Sci. USA 111, 4832–4837 (2014).
pubmed: 24616518
pmcid: 3977302
doi: 10.1073/pnas.1316513111
Sousa da Mota, B. et al. Imputation of ancient human genomes. Nat. Commun. 14, 3660 (2023).
pubmed: 37339987
pmcid: 10282092
doi: 10.1038/s41467-023-39202-0
Lawson, D. J., Hellenthal, G., Myers, S. & Falush, D. Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012).
pubmed: 22291602
pmcid: 3266881
doi: 10.1371/journal.pgen.1002453
Hellenthal, G. et al. A genetic atlas of human admixture history. Science 343, 747–751 (2014).
pubmed: 24531965
pmcid: 4209567
doi: 10.1126/science.1243518
Sikora, M. et al. The population history of northeastern Siberia since the Pleistocene. Nature 570, 182–188 (2019).
pubmed: 31168093
doi: 10.1038/s41586-019-1279-z
Shinde, V. et al. An ancient Harappan genome lacks ancestry from Steppe pastoralists or Iranian farmers. Cell 179, 729–735 (2019).
pubmed: 31495572
pmcid: 6800651
doi: 10.1016/j.cell.2019.08.048
Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886–6891 (2016).
pubmed: 27274049
pmcid: 4922144
doi: 10.1073/pnas.1523951113
Galinsky, K. J., Loh, P.-R., Mallick, S., Patterson, N. J. & Price, A. L. Population structure of UK Biobank and ancient Eurasians reveals adaptation at genes influencing blood pressure. Am. J. Hum. Genet. 99, 1130–1139 (2016).
pubmed: 27773431
pmcid: 5097941
doi: 10.1016/j.ajhg.2016.09.014
Patterson, N. et al. Large-scale migration into Britain during the Middle to Late Bronze Age. Nature 601, 588–594 (2022).
pubmed: 34937049
doi: 10.1038/s41586-021-04287-4
Olalde, I. et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Nature 555, 190–196 (2018).
pubmed: 29466337
pmcid: 5973796
doi: 10.1038/nature25738
Zaidi, A. A. & Mathieson, I. Demographic history mediates the effect of stratification on polygenic scores. eLife 9, e61548 (2020).
pubmed: 33200985
pmcid: 7758063
doi: 10.7554/eLife.61548
Jones, E. R. et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat. Commun. 6, 8912 (2015).
pubmed: 26567969
doi: 10.1038/ncomms9912
Speidel, L., Forest, M., Shi, S. & Myers, S. R. A method for genome-wide genealogy estimation for thousands of samples. Nat. Genet. 51, 1321–1329 (2019).
pubmed: 31477933
pmcid: 7610517
doi: 10.1038/s41588-019-0484-x
Speidel, L. et al. Inferring population histories for ancient genomes using genome-wide genealogies. Mol. Biol. Evol. 38, 3497–3511 (2021).
pubmed: 34129037
pmcid: 8383901
doi: 10.1093/molbev/msab174
Stern, A. J., Wilton, P. R. & Nielsen, R. An approximate full-likelihood method for inferring selection and allele frequency trajectories from DNA sequence data. PLoS Genet. 15, e1008384 (2019).
pubmed: 31518343
pmcid: 6760815
doi: 10.1371/journal.pgen.1008384
Buniello, A. et al. The NHGRI-EBI GWAS Catalog of published genome-wide association studies, targeted arrays and summary statistics 2019. Nucleic Acids Res. 47, D1005–D1012 (2019).
pubmed: 30445434
doi: 10.1093/nar/gky1120
1000 Genomes Project Consortium et al. A global reference for human genetic variation. Nature 526, 68–74 (2015).
doi: 10.1038/nature15393
Souilmi, Y. et al. Admixture has obscured signals of historical hard sweeps in humans. Nat. Ecol. Evol. 6, 2003–2015 (2022).
pubmed: 36316412
pmcid: 9715430
doi: 10.1038/s41559-022-01914-9
Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167–172 (2015).
pubmed: 26062507
doi: 10.1038/nature14507
Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015).
pubmed: 25731166
pmcid: 5048219
doi: 10.1038/nature14317
Enattah, N. S. et al. Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. Am. J. Hum. Genet. 82, 57–72 (2008).
pubmed: 18179885
pmcid: 2253962
doi: 10.1016/j.ajhg.2007.09.012
Itan, Y., Powell, A., Beaumont, M. A., Burger, J. & Thomas, M. G. The origins of lactase persistence in Europe. PLoS Comput. Biol. 5, e1000491 (2009).
pubmed: 19714206
pmcid: 2722739
doi: 10.1371/journal.pcbi.1000491
Ségurel, L. & Bon, C. On the evolution of lactase persistence in humans. Annu. Rev. Genomics Hum. Genet. 18, 297–319 (2017).
pubmed: 28426286
doi: 10.1146/annurev-genom-091416-035340
Segurel, L. et al. Why and when was lactase persistence selected for? Insights from Central Asian herders and ancient DNA. PLoS Biol. 18, e3000742 (2020).
pubmed: 32511234
pmcid: 7302802
doi: 10.1371/journal.pbio.3000742
Enattah, N. S. et al. Identification of a variant associated with adult-type hypolactasia. Nat. Genet. 30, 233–237 (2002).
pubmed: 11788828
doi: 10.1038/ng826
Wang, L. et al. A MicroRNA linking human positive selection and metabolic disorders. Cell 183, 684–701 (2020).
pubmed: 33058756
pmcid: 8092355
doi: 10.1016/j.cell.2020.09.017
Evershed, R. P. et al. Dairying, diseases and the evolution of lactase persistence in Europe. Nature 608, 336–345 (2022).
pubmed: 35896751
pmcid: 7615474
doi: 10.1038/s41586-022-05010-7
Mallick, S. et al. The Allen Ancient DNA Resource (AADR): a curated compendium of ancient human genomes. Preprint at bioRxiv https://doi.org/10.1101/2023.04.06.535797 (2023).
Willer, C. J. et al. Discovery and refinement of loci associated with lipid levels. Nat. Genet. 45, 1274–1283 (2013).
pubmed: 24097068
pmcid: 3838666
doi: 10.1038/ng.2797
Gallois, A. et al. A comprehensive study of metabolite genetics reveals strong pleiotropy and heterogeneity across time and context. Nat. Commun. 10, 4788 (2019).
pubmed: 31636271
pmcid: 6803661
doi: 10.1038/s41467-019-12703-7
Buckley, M. T. et al. Selection in Europeans on fatty acid desaturases associated with dietary changes. Mol. Biol. Evol. 34, 1307–1318 (2017).
pubmed: 28333262
pmcid: 5435082
doi: 10.1093/molbev/msx103
Ye, K., Gao, F., Wang, D., Bar-Yosef, O. & Keinan, A. Dietary adaptation of FADS genes in Europe varied across time and geography. Nat. Ecol. Evol. 1, 167 (2017).
pubmed: 29094686
pmcid: 5672832
doi: 10.1038/s41559-017-0167
Mathieson, S. & Mathieson, I. FADS1 and the timing of human adaptation to agriculture. Mol. Biol. Evol. 35, 2957–2970 (2018).
pubmed: 30272210
pmcid: 6278866
doi: 10.1093/molbev/msy180
Lazaridis, I. The evolutionary history of human populations in Europe. Curr. Opin. Genet. Dev. 53, 21–27 (2018).
pubmed: 29960127
doi: 10.1016/j.gde.2018.06.007
Luu, K., Bazin, E. & Blum, M. G. B. pcadapt: an R package to perform genome scans for selection based on principal component analysis. Mol. Ecol. Resour. 17, 67–77 (2017).
pubmed: 27601374
doi: 10.1111/1755-0998.12592
Sánchez-Solana, B., Li, D.-Q. & Kumar, R. Cytosolic functions of MORC2 in lipogenesis and adipogenesis. Biochim. Biophys. Acta 1843, 316–326 (2014).
pubmed: 24286864
doi: 10.1016/j.bbamcr.2013.11.012
Kim, S. V. et al. GPR15-mediated homing controls immune homeostasis in the large intestine mucosa. Science 340, 1456–1459 (2013).
pubmed: 23661644
pmcid: 3762262
doi: 10.1126/science.1237013
Nguyen, L. P. et al. Role and species-specific expression of colon T cell homing receptor GPR15 in colitis. Nat. Immunol. 16, 207–213 (2015).
Monteleone, G. et al. Mongersen, an oral SMAD7 antisense oligonucleotide and Crohn’s disease. N. Engl. J. Med. 372, 1104–1113 (2015).
pubmed: 25785968
doi: 10.1056/NEJMoa1407250
Kurki, M. I. et al. FinnGen provides genetic insights from a well-phenotyped isolated population. Nature 613, 508–518 (2023).
pubmed: 36653562
pmcid: 9849126
doi: 10.1038/s41586-022-05473-8
Morris, J. A. et al. An atlas of genetic influences on osteoporosis in humans and mice. Nat. Genet. 51, 258–266 (2018).
pubmed: 30598549
pmcid: 6358485
doi: 10.1038/s41588-018-0302-x
Brinkworth, J. F. & Barreiro, L. B. The contribution of natural selection to present-day susceptibility to chronic inflammatory and autoimmune disease. Curr. Opin. Immunol. 31, 66–78 (2014).
pubmed: 25458997
pmcid: 4344185
doi: 10.1016/j.coi.2014.09.008
Barrie, W. et al. Elevated genetic risk for multiple sclerosis emerged in steppe pastoralist populations. Nature https://doi.org/10.1038/s41586-023-06618-z (2024).
Jones, A. V. et al. GWAS of self-reported mosquito bite size, itch intensity and attractiveness to mosquitoes implicates immune-related predisposition loci. Hum. Mol. Genet. 26, 1391–1406 (2017).
pubmed: 28199695
pmcid: 5390679
doi: 10.1093/hmg/ddx036
Gutierrez-Achury, J. et al. Functional implications of disease-specific variants in loci jointly associated with coeliac disease and rheumatoid arthritis. Hum. Mol. Genet. 25, 180–190 (2016).
pubmed: 26546613
doi: 10.1093/hmg/ddv455
Stefansson, H. et al. A common inversion under selection in Europeans. Nat. Genet. 37, 129–137 (2005).
pubmed: 15654335
doi: 10.1038/ng1508
Steinberg, K. M. et al. Structural diversity and African origin of the 17q21.31 inversion polymorphism. Nat. Genet. 44, 872–880 (2012).
pubmed: 22751100
pmcid: 3408829
doi: 10.1038/ng.2335
Kılınç, G. M. et al. The demographic development of the first farmers in Anatolia. Curr. Biol. 26, 2659–2666 (2016).
pubmed: 27498567
pmcid: 5069350
doi: 10.1016/j.cub.2016.07.057
Broushaki, F. et al. Early Neolithic genomes from the eastern Fertile Crescent. Science 353, 499–503 (2016).
pubmed: 27417496
pmcid: 5113750
doi: 10.1126/science.aaf7943
Jones, E. R. et al. The Neolithic transition in the Baltic was not driven by admixture with early European farmers. Curr. Biol. 27, 576–582 (2017).
pubmed: 28162894
pmcid: 5321670
doi: 10.1016/j.cub.2016.12.060
Andreadis, A., Brown, W. M. & Kosik, K. S. Structure and novel exons of the human tau gene. Biochemistry 31, 10626–10633 (1992).
pubmed: 1420178
doi: 10.1021/bi00158a027
Jansen, P. R. et al. Genome-wide analysis of insomnia in 1,331,010 individuals identifies new risk loci and functional pathways. Nat. Genet. 51, 394–403 (2019).
pubmed: 30804565
doi: 10.1038/s41588-018-0333-3
Desikan, R. S. et al. Genetic overlap between Alzheimer’s disease and Parkinson’s disease at the MAPT locus. Mol. Psychiatry 20, 1588–1595 (2015).
pubmed: 25687773
pmcid: 4539304
doi: 10.1038/mp.2015.6
Aoki, K. Sexual selection as a cause of human skin colour variation: Darwin’s hypothesis revisited. Ann. Hum. Biol. 29, 589–608 (2002).
pubmed: 12573076
doi: 10.1080/0301446021000019144
Lona-Durazo, F. et al. Meta-analysis of GWA studies provides new insights on the genetic architecture of skin pigmentation in recently admixed populations. BMC Genet. 20, 59 (2019).
pubmed: 31315583
pmcid: 6637524
doi: 10.1186/s12863-019-0765-5
Jablonski, N. G. & Chaplin, G. The evolution of human skin coloration. J. Hum. Evol. 39, 57–106 (2000).
pubmed: 10896812
doi: 10.1006/jhev.2000.0403
Engelsen, O. The relationship between ultraviolet radiation exposure and vitamin D status. Nutrients 2, 482–495 (2010).
pubmed: 22254036
pmcid: 3257661
doi: 10.3390/nu2050482
Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. A map of recent positive selection in the human genome. PLoS Biol. 4, e72 (2006).
pubmed: 16494531
pmcid: 1382018
doi: 10.1371/journal.pbio.0040072
Martin, A. R. et al. An unexpectedly complex architecture for skin pigmentation in Africans. Cell 171, 1340–1353 (2017).
pubmed: 29195075
pmcid: 5884124
doi: 10.1016/j.cell.2017.11.015
Wu, H. et al. Transcriptome sequencing to detect the potential role of long noncoding RNAs in salt-sensitive hypertensive rats. BioMed Res. Int. 2019, 2816959 (2019).
pubmed: 31886193
pmcid: 6925802
doi: 10.1155/2019/2816959
Wang, L. et al. Peakwide mapping on chromosome 3q13 identifies the kalirin gene as a novel candidate gene for coronary artery disease. Am. J. Hum. Genet. 80, 650–663 (2007).
Zhang, K. et al. Genetic implication of a novel thiamine transporter in human hypertension. J. Am. Coll. Cardiol. 63, 1542–1555 (2014).
pubmed: 24509276
pmcid: 3992204
doi: 10.1016/j.jacc.2014.01.007
Zang, X.-L. et al. Association of a SNP in SLC35F3 gene with the risk of hypertension in a Chinese Han population. Front. Genet. 7, 108 (2016).
Russo, L. et al. Cholesterol 25-hydroxylase (CH25H) as a promoter of adipose tissue inflammation in obesity and diabetes. Mol. Metab. 39, 100983 (2020).
pubmed: 32229247
pmcid: 7267735
doi: 10.1016/j.molmet.2020.100983
Demir, A., Kahraman, R., Candan, G. & Ergen, A. The role of FAS gene variants in inflammatory bowel disease. Turk. J. Gastroenterol. 31, 356–361 (2020).
pubmed: 32519954
pmcid: 7289171
doi: 10.5152/tjg.2020.19436
Izawa, T. et al. ASXL2 regulates glucose, lipid and skeletal homeostasis. Cell Rep. 11, 1625–1637 (2015).
pubmed: 26051940
pmcid: 4472564
doi: 10.1016/j.celrep.2015.05.019
Vazirani, R. P. et al. Disruption of adipose Rab10-dependent insulin signaling causes hepatic insulin resistance. Diabetes 65, 1577–1589 (2016).
pubmed: 27207531
pmcid: 4878419
doi: 10.2337/db15-1128
Thapa, D. et al. The protein acetylase GCN5L1 modulates hepatic fatty acid oxidation activity via acetylation of the mitochondrial β-oxidation enzyme HADHA. J. Biol. Chem. 293, 17676–17684 (2018).
pubmed: 30323061
pmcid: 6240879
doi: 10.1074/jbc.AC118.005462
Ong, H. S. & Yim, H. C. H. in Regulation of Inflammatory Signaling in Health and Disease (ed. Xu, D.) 153–174 (Springer, 2017).
Girirajan, S., Campbell, C. D. & Eichler, E. E. Human copy number variation and complex genetic disease. Annu. Rev. Genet. 45, 203–226 (2011).
pubmed: 21854229
pmcid: 6662611
doi: 10.1146/annurev-genet-102209-163544
Weise, A. et al. Microdeletion and microduplication syndromes. J. Histochem. Cytochem. 60, 346–358 (2012).
pubmed: 22396478
pmcid: 3351230
doi: 10.1369/0022155412440001
Girirajan, S. et al. Phenotypic heterogeneity of genomic disorders and rare copy-number variants. N. Engl. J. Med. 367, 1321–1331 (2012).
pubmed: 22970919
pmcid: 3494411
doi: 10.1056/NEJMoa1200395
Mallick, S. et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538, 201–206 (2016).
pubmed: 27654912
pmcid: 5161557
doi: 10.1038/nature18964
Bergström, A. et al. Insights into human genetic variation and population history from 929 diverse genomes. Science 367, eaay5012 (2020).
pubmed: 32193295
pmcid: 7115999
doi: 10.1126/science.aay5012
Sudmant, P. H. et al. Diversity of human copy number variation and multicopy genes. Science 330, 641–646 (2010).
pubmed: 21030649
pmcid: 3020103
doi: 10.1126/science.1197005
Crawford, K. et al. Medical consequences of pathogenic CNVs in adults: analysis of the UK Biobank. J. Med. Genet. 56, 131–138 (2019).
pubmed: 30343275
doi: 10.1136/jmedgenet-2018-105477
Martin, A. R. et al. Human demographic history impacts genetic risk prediction across diverse populations. Am. J. Hum. Genet. 100, 635–649 (2017).
pubmed: 28366442
pmcid: 5384097
doi: 10.1016/j.ajhg.2017.03.004
Corder, E. H. et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer’s disease in late onset families. Science 261, 921–923 (1993).
pubmed: 8346443
doi: 10.1126/science.8346443
Belloy, M. E., Napolioni, V. & Greicius, M. D. A quarter century of APOE and Alzheimer’s disease: progress to date and the path forward. Neuron 101, 820–838 (2019).
pubmed: 30844401
pmcid: 6407643
doi: 10.1016/j.neuron.2019.01.056
Kolbe, D. et al. Current allele distribution of the human longevity gene APOE in Europe can mainly be explained by ancient admixture. Aging Cell 22, e13819 (2023).
pubmed: 36951219
pmcid: 10186601
doi: 10.1111/acel.13819
Rosenstock, E. et al. Human stature in the Near East and Europe ca. 10,000–1000 BC: its spatiotemporal development in a Bayesian errors-in-variables model. Archaeol. Anthropol. Sci. 11, 5657–5690 (2019).
doi: 10.1007/s12520-019-00850-3
Field, Y. et al. Detection of human adaptation during the past 2000 years. Science 354, 760–764 (2016).
pubmed: 27738015
pmcid: 5182071
doi: 10.1126/science.aag0776
Chen, M. et al. Evidence of polygenic adaptation in Sardinia at height-associated loci ascertained from the Biobank Japan. Am. J. Hum. Genet. 107, 60–71 (2020).
pubmed: 32533944
pmcid: 7332648
doi: 10.1016/j.ajhg.2020.05.014
Howe, L. J. et al. Within-sibship genome-wide association analyses decrease bias in estimates of direct genetic effects. Nat. Genet. 54, 581–592 (2022).
pubmed: 35534559
pmcid: 9110300
doi: 10.1038/s41588-022-01062-7