Genomic history of the Sardinian population

Nature Genetics

Volumn 50, Issue 10, 2018, Pages 1426-1434

  Chiang, Charleston W K ^a,b,c   Marcus, Joseph H ^d   Sidore, Carlo ^e,f   Biddanda, Arjun ^d   Al Asadi, Hussein ^d   Zoledziewska, Magdalena ^e   Pitzalis, Maristella ^e   Busonero, Fabio ^e,f   Maschio, Andrea ^e   Pistis, Giorgio ^e,f   Steri, Maristella ^e   Angius, Andrea ^e   Lohmueller, Kirk E ^c   Abecasis, Goncalo R ^f   Schlessinger, David ^g   Cucca, Francesco ^e,h   Novembre, John ^d  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e Milan Unit   (Italy)

^f UNIVERSITY OF MICHIGAN   (United States)

^g NATIONAL INSTITUTE ON AGING   (United States)

^h UNIVERSITY OF SASSARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANCIENT DNA;

ADULT; AGRICULTURAL WORKER; ALLELE; ARTICLE; BRONZE AGE; CASE CONTROL STUDY; COHORT ANALYSIS; CONTROLLED STUDY; DEMOGRAPHY; FEMALE; GENE FREQUENCY; GENETIC VARIABILITY; GENOME-WIDE ASSOCIATION STUDY; HUMAN; MAJOR CLINICAL STUDY; MALE; MIGRATION; NEOLITHIC; POPULATION SIZE; POPULATION STRUCTURE; PRIORITY JOURNAL; SARDINIA; SINGLE NUCLEOTIDE POLYMORPHISM; STEPPE; Y CHROMOSOME HAPLOGROUP; EPIDEMIOLOGY; GENETIC VARIATION; HISTORY; ITALY; LONGITUDINAL STUDY; PHYLOGENY; POPULATION GENETICS; SOUTHERN EUROPE; STATISTICS AND NUMERICAL DATA;

CASE-CONTROL STUDIES; DEMOGRAPHY; FEMALE; GENE FREQUENCY; GENETIC VARIATION; GENETICS, POPULATION; GENOME-WIDE ASSOCIATION STUDY; HISTORY, ANCIENT; HUMAN MIGRATION; HUMANS; ITALY; LONGITUDINAL STUDIES; MALE; MEDITERRANEAN REGION; PHYLOGENY;

EID: 85053696179     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/s41588-018-0215-8     Document Type: Article

References (84)

1. Lettre, G. & Hirschhorn, J. N. Small island, big genetic discoveries. Nat. Genet. 47, 1224–1225 (2015)
2. Sidore, C. et al. Genome sequencing elucidates Sardinian genetic architecture and augments association analyses for lipid and blood inflammatory markers. Nat. Genet. 47, 1272–1281 (2015)
3. Naitza, S. et al. A genome-wide association scan on the levels of markers of inflammation in Sardinians reveals associations that underpin its complex regulation. PLoS Genet. 8, e1002480 (2012)
4. Zoledziewska, M. et al. Height-reducing variants and selection for short stature in Sardinia. Nat. Genet. 47, 1352–1356 (2015)
5. Steri, M. et al. Overexpression of the cytokine BAFF and autoimmunity risk. N. Engl. J. Med. 376, 1615–1626 (2017)
6. Cucca, F. et al. The distribution of DR4 haplotypes in Sardinia suggests a primary association of type I diabetes with DRB1 and DQB1 loci. Hum. Immunol. 43, 301–308 (1995)
7. Marrosu, M. G. et al. The co-inheritance of type 1 diabetes and multiple sclerosis in Sardinia cannot be explained by genotype variation in the HLA region alone. Hum. Mol. Genet. 13, 2919–2924 (2004)
8. Pugliatti, M. et al. The epidemiology of multiple sclerosis in Europe. Eur. J. Neurol. 13, 700–722 (2006)
9. Cao, A. & Galanello, R. Beta-thalassemia. Genet. Med. 12, 61–76 (2010)
10. Dyson, S. L., & Rowland, R. J. Archaeology and History in Sardinia from the Stone Age to the Middle Ages: Shepherds, Sailors, & Conquerors (University of Pennsylvania Museum of Archaeology and Anthropology: Philadelphia, PA, USA, 2007)
11. Cavalli-Sforza, L. L., Menozzi, P. & Piazza, A. The History and Geography of Human Genes (Princeton University Press: Princeton, NJ, USA, 1994)
12. Eaves, I. A. et al. The genetically isolated populations of Finland and Sardinia may not be a panacea for linkage disequilibrium mapping of common disease genes. Nat. Genet. 25, 320–323 (2000)
13. Calò, C. M., Melis, A., Vona, G. & Piras, I. S. Sardinian population (Italy): a genetic review. Int. J. Mod. Anthropol. 1, 39–64 (2008)
14. Cavalli-Sforza, L. L. & Piazza, A. Human genomic diversity in Europe: a summary of recent research and prospects for the future. Eur. J. Hum. Genet. 1, 3–18 (1993)
15. Barbujani, G. & Sokal, R. R. Zones of sharp genetic change in Europe are also linguistic boundaries. Proc. Natl Acad. Sci. USA 87, 1816–1819 (1990)
16. Zavattari, P. et al. Major factors influencing linkage disequilibrium by analysis of different chromosome regions in distinct populations: demography, chromosome recombination frequency and selection. Hum. Mol. Genet. 9, 2947–2957 (2000)
17. Elhaik, E. et al. Geographic population structure analysis of worldwide human populations infers their biogeographical origins. Nat. Commun. 5, 3513 (2014)
18. Cann, H. M. Human genome diversity. C. R. Acad. Sci. III, Sci. Vie 321, 443–446 (1998)
19. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015)
20. Keller, A. et al. New insights into the Tyrolean Iceman’s origin and phenotype as inferred by whole-genome sequencing. Nat. Commun. 3, 698 (2012)
21. Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014)
22. Li, J. Z. et al. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319, 1100–1104 (2008)
23. Skoglund, P. et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336, 466–469 (2012)
24. Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167–172 (2015)
25. Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886–6891 (2016)
26. Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015)
27. Sikora, M. et al. Population genomic analysis of ancient and modern genomes yields new insights into the genetic ancestry of the Tyrolean Iceman and the genetic structure of Europe. PLoS Genet. 10, e1004353 (2014)
28. Ghirotto, S. et al. Inferring genealogical processes from patterns of Bronze-Age and modern DNA variation in Sardinia. Mol. Biol. Evol. 27, 875–886 (2010)
29. Fraumene, C., Petretto, E., Angius, A. & Pirastu, M. Striking differentiation of sub-populations within a genetically homogeneous isolate (Ogliastra) in Sardinia as revealed by mtDNA analysis. Hum. Genet. 114, 1–10 (2003)
30. Morelli, L. et al. Frequency distribution of mitochondrial DNA haplogroups in Corsica and Sardinia. Hum. Biol. 72, 585–595 (2000)
31. Pala, M. et al. Mitochondrial haplogroup U5b3: a distant echo of the epipaleolithic in Italy and the legacy of the early Sardinians. Am. J. Hum. Genet. 84, 814–821 (2009)
32. Olivieri, A. et al. Mitogenome diversity in Sardinians: a genetic window onto an island’s past. Mol. Biol. Evol. 34, 1230–1239 (2017)
33. Francalacci, P. et al. Low-pass DNA sequencing of 1200 Sardinians reconstructs European Y-chromosome phylogeny. Science 341, 565–569 (2013)
34. Caramelli, D. et al. Genetic variation in prehistoric Sardinia. Hum. Genet. 122, 327–336 (2007)
35. Vona, G. The peopling of Sardinia (Italy): history and effects. Int. J. Anthropol. 12, 71–87 (1997)
36. Contu, D. et al. Y-chromosome based evidence for pre-neolithic origin of the genetically homogeneous but diverse Sardinian population: inference for association scans. PLoS One 3, e1430 (2008)
37. Morelli, L. et al. A comparison of Y-chromosome variation in Sardinia and Anatolia is more consistent with cultural rather than demic diffusion of agriculture. PLoS One 5, e10419 (2010)
38. Semino, O. et al. The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective. Science 290, 1155–1159 (2000)
39. Rootsi, S. et al. Phylogeography of Y-chromosome haplogroup I reveals distinct domains of prehistoric gene flow in europe. Am. J. Hum. Genet. 75, 128–137 (2004)
40. Chikhi, L., Nichols, R. A., Barbujani, G. & Beaumont, M. A. Y genetic data support the Neolithic demic diffusion model. Proc. Natl Acad. Sci. USA 99, 11008–11013 (2002)
41. Passarino, G. et al. Y chromosome binary markers to study the high prevalence of males in Sardinian centenarians and the genetic structure of the Sardinian population. Hum. Hered. 52, 136–139 (2001)
42. Olalde, I. et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Nature 555, 190–196 (2018)
43. Kivisild, T. The study of human Y chromosome variation through ancient DNA. Hum. Genet. 136, 529–546 (2017)
44. Skoglund, P. et al. Genomic insights into the peopling of the Southwest Pacific. Nature 538, 510–513 (2016)
45. Goldberg, A., Gunther, T., Rosenberg, N. A. & Jakobsson, M. Ancient X chromosomes reveal contrasting sex bias in Neolithic and Bronze Age Eurasian migrations. Proc. Natl Acad. Sci. USA 114, 2657–2662 (2017)
46. Günther, T. et al. Ancient genomes link early farmers from Atapuerca in Spain to modern-day Basques. Proc. Natl Acad. Sci. USA 112, 11917–11922 (2015)
47. Hellenthal, G. et al. A genetic atlas of human admixture history. Science 343, 747–751 (2014)
48. Loh, P. R. et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193, 1233–1254 (2013)
49. Moorjani, P. et al. The history of African gene flow into Southern Europeans, Levantines, and Jews. PLoS Genet. 7, e1001373 (2011)
50. Barbujani, G., Bertorelle, G., Capitani, G. & Scozzari, R. Geographical structuring in the mtDNA of Italians. Proc. Natl Acad. Sci. USA 92, 9171–9175 (1995)
51. Pistis, G. et al. High differentiation among eight villages in a secluded area of Sardinia revealed by genome-wide high density SNPs analysis. PLoS One 4, e4654 (2009)
52. Sanna, S. et al. Variants within the immunoregulatory CBLB gene are associated with multiple sclerosis. Nat. Genet. 42, 495–497 (2010)
53. Zoledziewska, M. et al. Variation within the CLEC16A gene shows consistent disease association with both multiple sclerosis and type 1 diabetes in Sardinia. Genes Immun. 10, 15–17 (2009)
54. Pilia, G. et al. Heritability of cardiovascular and personality traits in 6,148 Sardinians. PLoS Genet. 2, e132 (2006)
55. Petkova, D., Novembre, J. & Stephens, M. Visualizing spatial population structure with estimated effective migration surfaces. Nat. Genet. 48, 94–100 (2016)
56. Novembre, J. & Stephens, M. Interpreting principal component analyses of spatial population genetic variation. Nat. Genet. 40, 646–649 (2008)
57. Botigué, L. R. et al. Gene flow from North Africa contributes to differential human genetic diversity in southern Europe. Proc. Natl Acad. Sci. USA 110, 11791–11796 (2013)
58. Henn, B. M. et al. Genomic ancestry of North Africans supports back-to-Africa migrations. PLoS Genet. 8, e1002397 (2012)
59. Paschou, P. et al. Maritime route of colonization of Europe. Proc. Natl Acad. Sci. USA 111, 9211–9216 (2014)
60. Terhorst, J., Kamm, J. A. & Song, Y. S. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49, 303–309 (2017)
61. Schiffels, S. & Durbin, R. Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46, 919–925 (2014)
62. Raghavan, M. et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505, 87–91 (2014)
63. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012)
64. Blasco Ferrer, E. Paleosardo: Le Radici Linguistiche Della Sardegna Neolitica (De Gruyter, Berlin and New York, 2010)
65. Pickrell, J. K. et al. Ancient west Eurasian ancestry in southern and eastern Africa. Proc. Natl Acad. Sci. USA 111, 2632–2637 (2014)
66. Heyer, E., Chaix, R., Pavard, S. & Austerlitz, F. Sex-specific demographic behaviours that shape human genomic variation. Mol. Ecol. 21, 597–612 (2012)
67. Lazaridis, I. & Reich, D. Failure to replicate a genetic signal for sex bias in the steppe migration into central Europe. Proc. Natl Acad. Sci. USA 114, E3873–E3874 (2017)
68. Goldberg, A., Günther, T., Rosenberg, N. A. & Jakobsson, M. Reply to Lazaridis and Reich: robust model-based inference of male-biased admixture during Bronze Age migration from the Pontic-Caspian Steppe. Proc. Natl Acad. Sci. USA 114, E3875–E3877 (2017)
69. Wilkins, J. F. & Marlowe, F. W. Sex-biased migration in humans: what should we expect from genetic data? Bioessays 28, 290–300 (2006)
70. Keinan, A. & Clark, A. G. Recent explosive human population growth has resulted in an excess of rare genetic variants. Science 336, 740–743 (2012)
71. Joshi, P. K. et al. Directional dominance on stature and cognition in diverse human populations. Nature 523, 459–462 (2015)
72. Lohmueller, K. E. The impact of population demography and selection on the genetic architecture of complex traits. PLoS Genet. 10, e1004379 (2014)
73. Simons, Y. B., Turchin, M. C., Pritchard, J. K. & Sella, G. The deleterious mutation load is insensitive to recent population history. Nat. Genet. 46, 220–224 (2014)
74. Uricchio, L. H., Zaitlen, N. A., Ye, C. J., Witte, J. S. & Hernandez, R. D. Selection and explosive growth alter genetic architecture and hamper the detection of causal rare variants. Genome Res. 26, 863–873 (2016)
75. Browning, B. L. & Browning, S. R. A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am. J. Hum. Genet. 84, 210–223 (2009)
76. Altshuler, D. M. et al. Integrating common and rare genetic variation in diverse human populations. Nature 467, 52–58 (2010)
77. Price, A. L. et al. Long-range LD can confound genome scans in admixed populations. Am. J. Hum. Genet. 83, 135–139 (2008)
78. Kong, A. et al. Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467, 1099–1103 (2010)
79. Tennessen, J. A. et al. Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337, 64–69 (2012)
80. Gravel, S. et al. Demographic history and rare allele sharing among human populations. Proc. Natl Acad. Sci. USA 108, 11983–11988 (2011)
81. Nelson, M. R. et al. An abundance of rare functional variants in 202 drug target genes sequenced in 14,002 people. Science 337, 100–104 (2012)
82. Shringarpure, S. S., Bustamante, C. D., Lange, K. & Alexander, D. H. Efficient analysis of large datasets and sex bias with ADMIXTURE. BMC Bioinformatics 17, 218 (2016)
83. Mallick, S. et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538, 201–206 (2016)
84. Woerner, A. E., Veeramah, K. R., Watkins, J. C., Hammer, M. F. & Novembre, J. The role of phylogenetically conserved elements in shaping patterns of human genomic diversity. Mol. Biol. Evol. 35, 2284–2295 (2018)