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Maternal History of Oceania from Complete mtDNA Genomes: Contrasting Ancient Diversity with Recent Homogenization Due to the Austronesian Expansion

2014; Elsevier BV; Volume: 94; Issue: 5 Linguagem: Inglês

10.1016/j.ajhg.2014.03.014

1537-6605

Ana T. Duggan, Bethwyn Evans, Françoise R. Friedlaender, Jonathan S. Friedlaender, George Koki, D. Andrew Merriwether, Manfred Kayser, Mark Stoneking,

Genetic diversity and population structure

Archaeology, linguistics, and existing genetic studies indicate that Oceania was settled by two major waves of migration. The first migration took place approximately 40 thousand years ago and these migrants, Papuans, colonized much of Near Oceania. Approximately 3.5 thousand years ago, a second expansion of Austronesian-speakers arrived in Near Oceania and the descendants of these people spread to the far corners of the Pacific, colonizing Remote Oceania. To assess the female contribution of these two human expansions to modern populations and to investigate the potential impact of other migrations, we obtained 1,331 whole mitochondrial genome sequences from 34 populations spanning both Near and Remote Oceania. Our results quantify the magnitude of the Austronesian expansion and demonstrate the homogenizing effect of this expansion on almost all studied populations. With regards to Papuan influence, autochthonous haplogroups support the hypothesis of a long history in Near Oceania, with some lineages suggesting a time depth of 60 thousand years, and offer insight into historical interpopulation dynamics. Santa Cruz, a population located in Remote Oceania, is an anomaly with extreme frequencies of autochthonous haplogroups of Near Oceanian origin; simulations to investigate whether this might reflect a pre-Austronesian versus Austronesian settlement of the island failed to provide unequivocal support for either scenario. Archaeology, linguistics, and existing genetic studies indicate that Oceania was settled by two major waves of migration. The first migration took place approximately 40 thousand years ago and these migrants, Papuans, colonized much of Near Oceania. Approximately 3.5 thousand years ago, a second expansion of Austronesian-speakers arrived in Near Oceania and the descendants of these people spread to the far corners of the Pacific, colonizing Remote Oceania. To assess the female contribution of these two human expansions to modern populations and to investigate the potential impact of other migrations, we obtained 1,331 whole mitochondrial genome sequences from 34 populations spanning both Near and Remote Oceania. Our results quantify the magnitude of the Austronesian expansion and demonstrate the homogenizing effect of this expansion on almost all studied populations. With regards to Papuan influence, autochthonous haplogroups support the hypothesis of a long history in Near Oceania, with some lineages suggesting a time depth of 60 thousand years, and offer insight into historical interpopulation dynamics. Santa Cruz, a population located in Remote Oceania, is an anomaly with extreme frequencies of autochthonous haplogroups of Near Oceanian origin; simulations to investigate whether this might reflect a pre-Austronesian versus Austronesian settlement of the island failed to provide unequivocal support for either scenario. Within the boundaries of Oceania, one of the first and one of the last major colonization events by anatomically modern humans occurred. Settlement of New Guinea and Australia, which were then joined as a single landmass known as Sahul, occurred at least 44 kiloannum (ka) ago1Groube L. Chappell J. Muke J. Price D. A 40,000 year-old human occupation site at Huon Peninsula, Papua New Guinea.Nature. 1986; 324: 453-455Crossref PubMed Scopus (208) Google Scholar, 2Summerhayes G.R. Leavesley M. Fairbairn A. Mandui H. Field J. Ford A. Fullagar R. 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Pleistocene human occupation of the Solomon Islands, Melanesia.Antiquity. 1988; 62: 703-706Google Scholar and Manus in the Admiralty Islands by 12 ka ago,6Fredericksen C. Spriggs M. Ambrose W. Pamwak rockshelter: a pleistocene site on Manus Island, Papua New Guinea.in: Smith M.A. Spriggs M. Frankhauser B. Sahul in Review: Pleistocene Archaeology in Australia, New Guinea and Island Melanesia. Australian National University, Canberra1993: 144-154Google Scholar indicating that they possessed sufficient watercraft and sailing skills to voyage at least 200 km. However, there are no indications that they made regular long-distance voyages beyond Near Oceania,7Kirch P.V. On the Road of the Winds-An Archaeological History of the Pacific Islands Before European Contact. University of California Press, Berkeley2000Google Scholar which comprises New Guinea, the Bismarck Archipelago, and the Solomon Islands as far southeast as Makira. 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People believed to be descended from the first expansion within Near Oceania are often referred to as Papuan, generally practice patrilocality, tend to have darker skin pigmentation reflecting the root of the region's historical name—Melanesia—as the "dark islands,"7Kirch P.V. On the Road of the Winds-An Archaeological History of the Pacific Islands Before European Contact. University of California Press, Berkeley2000Google Scholar and speak languages that appear to be so old and deep rooting that linguists are still unsure about their true relationships.19Pawley A. Recent research on the historical relationships of the Papuan languages, or, what does linguistics say about the prehistory of Melanesia.in: Friedlaender J.S. Genes, Language, and Culture History in the Southwest Pacific. Oxford University Press, New York2007: 36-58Google Scholar, 20Hunley K. Dunn M. Lindström E. Reesink G. Terrill A. Norton H. Scheinfeldt L. Friedlaender F.R. Merriwether D.A. Koki G. Friedlaender J.S. Inferring prehistory from genetic, linguistic, and geographic variation.in: Friedlaender J.S. Genes, Language and Culture History in the Southwest Pacific. Oxford University Press, New York2007: 141-154Google Scholar By contrast, the second migration into Near Oceania is indicated by the presence of a particular material culture, including, but not limited to, a distinctive style of pottery (Lapita) and is associated with speakers of Austronesian languages that are clearly related and descended from a single language called Proto Oceanic (see Lynch et al.21Lynch J. Ross M. Crowley T. The Oceanic Languages. Curzon Press, Richmond, Surrey2002Google Scholar and references therein). Reconstructions suggest they lived in small, highly mobile matrilocal groups22Jordan F.M. Gray R.D. Greenhill S.J. Mace R. Matrilocal residence is ancestral in Austronesian societies.Proc. Biol. Sci. 2009; 276: 1957-1964Crossref PubMed Scopus (135) Google Scholar and were phenotypically more similar to Asian populations (e.g., with generally lighter skin pigmentation) than are Papuans. We can also make genetic ties to both of these founding populations. The Austronesian expansion is associated with the spread of mtDNA haplogroup B, particularly haplogroup B4a1 and its descendent lineages, throughout Island South East Asia, Oceania, and even to Madagascar in the west.10Trejaut J.A. Kivisild T. Loo J.H. Lee C.L. He C.L. Hsu C.J. Lee Z.Y. Lin M. Traces of archaic mitochondrial lineages persist in Austronesian-speaking Formosan populations.PLoS Biol. 2005; 3: e247Crossref PubMed Scopus (179) Google Scholar, 23Soodyall H. Jenkins T. Stoneking M. 'Polynesian' mtDNA in the Malagasy.Nat. Genet. 1995; 10: 377-378Crossref PubMed Scopus (46) Google Scholar, 24Kayser M. Brauer S. Cordaux R. Casto A. Lao O. Zhivotovsky L.A. Moyse-Faurie C. Rutledge R.B. Schiefenhoevel W. 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Rutledge R.B. Schiefenhoevel W. Gil D. et al.Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific.Mol. Biol. Evol. 2006; 23: 2234-2244Crossref PubMed Scopus (187) Google Scholar, 29Melton T. Peterson R. Redd A.J. Saha N. Sofro A.S. Martinson J. Stoneking M. Polynesian genetic affinities with Southeast Asian populations as identified by mtDNA analysis.Am. J. Hum. Genet. 1995; 57: 403-414Crossref PubMed Scopus (36) Google Scholar, 30Redd A.J. Takezaki N. Sherry S.T. McGarvey S.T. Sofro A.S. Stoneking M. Evolutionary history of the COII/tRNALys intergenic 9 base pair deletion in human mitochondrial DNAs from the Pacific.Mol. Biol. Evol. 1995; 12: 604-615PubMed Google Scholar though position 16247 has been found to back-mutate repeatedly on independent lineages and as such must be examined carefully.31Duggan A.T. Stoneking M. A highly unstable recent mutation in human mtDNA.Am. J. Hum. Genet. 2013; 92: 279-284Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar Meanwhile, Papuan ancestry is associated with haplogroups Q, P, M27, M28, and M29, which appear to be autochthonous to Near Oceania.24Kayser M. Brauer S. Cordaux R. Casto A. Lao O. Zhivotovsky L.A. Moyse-Faurie C. Rutledge R.B. Schiefenhoevel W. Gil D. et al.Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific.Mol. Biol. Evol. 2006; 23: 2234-2244Crossref PubMed Scopus (187) Google Scholar, 32Friedlaender J. Schurr T. Gentz F. Koki G. Friedlaender F. Horvat G. Babb P. Cerchio S. Kaestle F. Schanfield M. et al.Expanding Southwest Pacific mitochondrial haplogroups P and Q.Mol. Biol. Evol. 2005; 22: 1506-1517Crossref PubMed Scopus (95) Google Scholar, 33Merriwether D.A. Hodgson J.A. Friedlaender F.R. Allaby R. Cerchio S. Koki G. Friedlaender J.S. Ancient mitochondrial M haplogroups identified in the Southwest Pacific.Proc. Natl. Acad. Sci. 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In this study, we examined the maternal population structure and the history of admixture across Oceania. Previous studies exploring the maternal histories of the area have been limited because they largely make use of only a small portion of the genome known as the hypervariable region (HVR) (e.g., see Kayser et al.,24Kayser M. Brauer S. Cordaux R. Casto A. Lao O. Zhivotovsky L.A. Moyse-Faurie C. Rutledge R.B. Schiefenhoevel W. Gil D. et al.Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific.Mol. Biol. Evol. 2006; 23: 2234-2244Crossref PubMed Scopus (187) Google Scholar Friedlaender et al.,25Friedlaender J.S. Friedlaender F.R. Hodgson J.A. Stoltz M. Koki G. Horvat G. Zhadanov S. Schurr T.G. Merriwether D.A. Melanesian mtDNA complexity.PLoS ONE. 2007; 2: e248https://doi.org/10.1371/journal.pone.0000248Crossref PubMed Scopus (96) Google Scholar Delfin et al.41Delfin F. Myles S. Choi Y. Hughes D. Illek R. van Oven M. Pakendorf B. Kayser M. 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Our data set is, to our knowledge, the most comprehensive to date, and consists of 1,331 whole mitochondrial genome sequences from 34 populations spread from the Bismarck Archipelago to Polynesia (Figure 1). To facilitate comprehension and visualization of the patterns of variation, these 34 populations have been amalgamated into six groups on the basis of geographic proximity and/or shared cultural features (Figure 1). The first group consists of populations from New Britain in the Bismarck Archipelago (Anem, Ata, Nakanai) and the second group consists of populations from Bougainville and Buka (Buin, Buka, Nagovisi, Nasioi, Siwai, Torau), two islands at the northern tip of the Solomons Archipelago that politically are part of Papua New Guinea, and the easternmost site of known settlement in Pleistocene Oceania.5Wickler S. Spriggs M. Pleistocene human occupation of the Solomon Islands, Melanesia.Antiquity. 1988; 62: 703-706Google Scholar The only other confirmed pre-Austronesian settlements in the Solomons Archipelago are sites from Guadalcanal with indications of human occupation approximately 6 ka ago.44Roe D. Prehistory without pots: prehistoric settlement and economy of North-west Guadalcanal, Solomon Islands. PhD thesis. Australian National University, Canberra1993Google Scholar, 45Walter R. Sheppard P. A review of Solomon Islands archaeology.in: Sheppard P. Thomas T. Summerhayes G. Lapita: Ancestors and Descendants. New Zealand Archaeological Association, Auckland2009: 35-72Google Scholar The third group consists of populations found in the islands of the rest of the Solomons Archipelago (Choiseul, Gela, Guadalcanal, Isabel, Kolombangara, Makira, Malaita, Ranongga, Russell, Savo, Shortlands, Simbo, Vella Lavella). Santa Cruz is the only population to be grouped alone; it is treated separately because it has been shown to be a genetic outlier in previous studies of mtDNA and Y chromosome variation41Delfin F. Myles S. Choi Y. Hughes D. Illek R. van Oven M. Pakendorf B. Kayser M. Stoneking M. Bridging near and remote Oceania: mtDNA and NRY variation in the Solomon Islands.Mol. Biol. Evol. 2012; 29: 545-564Crossref PubMed Scopus (45) Google Scholar, 46Friedlaender J.S. Gentz F. Green K. Merriwether D.A. A cautionary tale on ancient migration detection: mitochondrial DNA variation in Santa Cruz Islands, Solomon Islands.Hum. Biol. 2002; 74: 453-471Crossref PubMed Scopus (31) Google Scholar as well as being linguistically distinct. Originally classified as a Papuan language, currently the Santa Cruz language and closely related languages of the Temotu group are thought to represent a very deep branch of the Oceanic family of Austronesian languages.47Ross M. Næss Å. 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Lao O. Zhivotovsky L.A. Moyse-Faurie C. Rutledge R.B. Schiefenhoevel W. Gil D. et al.Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific.Mol. Biol. Evol. 2006; 23: 2234-2244Crossref PubMed Scopus (187) Google Scholar, 34Kayser M. Brauer S. Weiss G. Underhill P.A. Roewer L. Schiefenhövel W. Stoneking M. Melanesian origin of Polynesian Y chromosomes.Curr. Biol. 2000; 10: 1237-1246Abstract Full Text Full Text PDF PubMed Scopus (163) Google Scholar, 41Delfin F. Myles S. Choi Y. Hughes D. Illek R. van Oven M. Pakendorf B. Kayser M. Stoneking M. Bridging near and remote Oceania: mtDNA and NRY variation in the Solomon Islands.Mol. Biol. Evol. 2012; 29: 545-564Crossref PubMed Scopus (45) Google Scholar, 52Trent R.J. Mickleson K.N. Wilkinson T. Yakas J. Dixon M.W. Hill P.J. Kronenberg H. Globin genes in Polynesians have many rearrangements including a recently described gamma gamma gamma gamma/.Am. J. Hum. 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BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.Nucleic Acids Symp. Ser. 1999; 41: 95-98Google Scholar Heteroplasmies and indels were confirmed with SAMtools.59Li H. Handsaker B. Wysoker A. Fennell T. Ruan J. Homer N. Marth G. Abecasis G. Durbin R. 1000 Genome Project Data Processing SubgroupThe Sequence Alignment/Map format and SAMtools.Bioinformatics. 2009; 25: 2078-2079Crossref PubMed Scopus (31559) Google Scholar There are no significant differences in the number of variant sites called per sequence with respect to coverage or sequencing platform. 536 sequences from the Solomon Islands, Santa Cruz, and Polynesian Outlier populations that belong to haplogroup B4a1a1 and descendent lineages were previously published as part of a study on the instability of the 16247G allele.31Duggan A.T. Stoneking M. A highly unstable recent mutation in human mtDNA.Am. J. Hum. Genet. 2013; 92: 279-284Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar Haplogroups were assigned to consensus sequences for each sample with the Haplogrep webtool and Phylotree Build 15.60van Oven M. Kayser M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation.Hum. Mutat. 2009; 30: