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Genomic insights into population history and biological adaptation in Oceania Jeremy Choin, Javier Mendoza-Revilla, Lara Arauna, Sebastian Cuadros-Espinoza, Olivier Cassar, Maximilian Larena, Albert Min-Shan Ko, Christine Harmant, Romain Laurent, Paul Verdu, et al. To cite this version: Jeremy Choin, Javier Mendoza-Revilla, Lara Arauna, Sebastian Cuadros-Espinoza, Olivier Cassar, et al.. Genomic insights into population history and biological adaptation in Oceania. Nature, Nature Publishing Group, 2021, 592 (7855), pp.583-589. 10.1038/s41586-021-03236-5. pasteur-03205291 HAL Id: pasteur-03205291 https://hal-pasteur.archives-ouvertes.fr/pasteur-03205291 Submitted on 11 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Article Genomic insights into population history and biological adaptation in Oceania https://doi.org/10.1038/s41586-021-03236-5 Jeremy Choin1,2,16, Javier Mendoza-Revilla1,16, Lara R. Arauna1,16, Sebastian Cuadros-Espinoza1,3, Olivier Cassar4, Maximilian Larena5, Albert Min-Shan Ko6, Christine Harmant1, Romain Laurent7, Received: 20 May 2020 Paul Verdu7, Guillaume Laval1, Anne Boland8, Robert Olaso8, Jean-François Deleuze8, Accepted: 13 January 2021 Frédérique Valentin9, Ying-Chin Ko10, Mattias Jakobsson5,11, Antoine Gessain4, Laurent Excoffier12,13, Mark Stoneking14, Etienne Patin1,17 ✉ & Lluis Quintana-Murci1,15,17 ✉ Published online: 14 April 2021 Check for updates The Pacifc region is of major importance for addressing questions regarding human dispersals, interactions with archaic hominins and natural selection processes1. However, the demographic and adaptive history of Oceanian populations remains largely uncharacterized. Here we report high-coverage genomes of 317 individuals from 20 populations from the Pacifc region. We fnd that the ancestors of Papuan-related (‘Near Oceanian’) groups underwent a strong bottleneck before the settlement of the region, and separated around 20,000–40,000 years ago. We infer that the East Asian ancestors of Pacifc populations may have diverged from Taiwanese Indigenous peoples before the Neolithic expansion, which is thought to have started from Taiwan around 5,000 years ago2–4. Additionally, this dispersal was not followed by an immediate, single admixture event with Near Oceanian populations, but involved recurrent episodes of genetic interactions. Our analyses reveal marked diferences in the proportion and nature of Denisovan heritage among Pacifc groups, suggesting that independent interbreeding with highly structured archaic populations occurred. Furthermore, whereas introgression of Neanderthal genetic information facilitated the adaptation of modern humans related to multiple phenotypes (for example, metabolism, pigmentation and neuronal development), Denisovan introgression was primarily benefcial for immune-related functions. Finally, we report evidence of selective sweeps and polygenic adaptation associated with pathogen exposure and lipid metabolism in the Pacifc region, increasing our understanding of the mechanisms of biological adaptation to island environments. Archaeological data indicate that Near Oceania, which includes New Guinea, island environments, and whether archaic introgression facilitated this the Bismarck archipelago and the Solomon Islands, was peopled around process in Oceanian individuals, who present the highest levels of com- 45 thousand years ago (ka)5.The rest of the Pacific—known as Remote Oce- bined Neanderthal and Denisovan ancestry worldwide14–17. We report here ania, and including Micronesia, Santa Cruz, Vanuatu, New Caledonia, Fiji a whole-genome-based survey that addresses a wide range of questions and Polynesia—was not settled until around 35 thousand years later. This relating to the demographic and adaptive history of Pacific populations. dispersal, associated with the spread of Austronesian languages and the Lapita cultural complex, is thought to have started in Taiwan around 5 ka, reaching Remote Oceania by about 0.8–3.2 ka6. Although genetic studies Genomic dataset and population structure of Oceanian populations have revealed admixture with populations of We sequenced the genomes of 317 individuals from 20 populations East Asian origin7–13, attributed to the Austronesian expansion, questions spanning a geographical transect that is thought to underlie the regarding the peopling history of Oceania remain. It is also unknown how peopling history of Near and Remote Oceania (Fig. 1a and Supple- the settlement of the Pacific was accompanied by genetic adaptation to mentary Note 1). These high-coverage genomes (around 36×) were 1Human Evolutionary Genetics Unit, Institut Pasteur, UMR 2000, CNRS, Paris, France. 2Université Paris Diderot, Sorbonne Paris Cité, Paris, France. 3Sorbonne Université, Collège doctoral, Paris, France. 4Oncogenic Virus Epidemiology and Pathophysiology, Institut Pasteur, UMR 3569, CNRS, Paris, France. 5Human Evolution, Department of Organismal Biology, Uppsala University, Uppsala, Sweden. 6Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China. 7Muséum National d’Histoire Naturelle, UMR7206, CNRS, Université de Paris, Paris, France. 8Centre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François Jacob, CEA, Université Paris-Saclay, Evry, France. 9Maison de l’Archéologie et de l’Ethnologie, UMR 7041, CNRS, Nanterre, France. 10Environment-Omics-Disease Research Center, China Medical University and Hospital, Taichung, Taiwan. 11Science for Life Laboratory, Uppsala University, Uppsala, Sweden. 12Institute of Ecology and Evolution, University of Bern, Bern, Switzerland. 13Swiss Institute of Bioinformatics, Lausanne, Switzerland. 14Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany. 15Collège de France, Paris, France. 16These authors contributed equally: Jeremy Choin, Javier Mendoza-Revilla, Lara R. Arauna. 17These authors jointly supervised this work: Etienne Patin, Lluis Quintana-Murci. ✉e-mail: [email protected]; [email protected] Nature | Vol 592 | 22 April 2021 | 583 Article a SantaCruz (14) b All genomes dbSNP ) 7 New genomes Tikopia (10) New genomes New variants Ureparapara (20) 4 Atayal (10) Ambae (15) 20° N Maewo (8) Paiwan (9) Agta (20) Santo (20) Pentecost 3 (20) of SNPs (×10 549.8 1.24 0. Malakula (20) Ambrym 2 10° N Cebuano (20) (20) Emae (15) 1 Efate (21) Tanna (20) Number 0° 0 Latitude Malaita (18) d 0.15 10° S Vella Lavella Polynesians (18) 0.10 Near and western Rennell (4) Remote Oceanians 20° S Bellona (15) 0.05 0 East/Southeast 110° W 130° W 150° W 170° W PC2 (1.8%) Asians c Longitude –0.05 Australians –0.10 –0.10 –0.05 00.05 20° N PC1 (6.3%) e ) 8.0 10° N –4 7.5 0° Latitude 7.0 10° S Heterozygosity (×10 6.5 20° S l a z 110° W 130° W 150° W 170° W n u o Agta anai uano k alaita Cr anna Ataya b Bundi ikopia T Longitude Paiwan ndiawa Lavella M T alakula u Na Ce a M K ll Taiwanese Indigenous peoples Australians Bismarck Islanders SantaCruz Islanders Santa Ve Philippine populations Papua New Guinea Bougainville Islanders Ni-Vanuatu Renell Bell Malaysians Highlanders Solomon Islanders Polynesians Fig. 1 | Whole-genome variation in Pacific Islanders. a, Location of studied all K values, see Extended Data Fig. 1). ADMIXTURE results for Australian populations. The indented map is a magnification of western Remote Oceania. populations are discussed in Supplementary Note 3. d, PCA of Pacific Islanders Circles indicate newly generated genomes. Sample sizes are indicated in and East Asian individuals. The proportion of variance explained is indicated in parentheses. Squares, triangles and diamonds indicate genomes from Mallick parentheses. e, Population levels of heterozygosity (for all populations, see et al.19, Vernot et al.16 and Malaspinas et al.18, respectively. b, The number of Supplementary Fig. 9). Population samples were randomly down-sampled to SNPs (left), expressed in tens of millions, and comparison with dbSNP (right). obtain equal sizes (n = 5). The line, box, whiskers and points indicate the New variants are SNPs that are absent from available datasets16,18,19 and dbSNP. median, interquartile range, 1.5× the interquartile range and outliers, c, ADMIXTURE ancestry proportions at K = 6 (lowest cross-validation error; for respectively. a, c, Maps were generated using the maps R package51. analysed with the genomes of selected populations—including Papua probably reflect low effective population sizes. Notably, F-statistics New Guinean Highlanders and Bismarck Islanders16,18,19—and archaic show a higher genetic affinity of ni-Vanuatu from Emae to Polynesian hominins20–22 (Supplementary Note 2 and Supplementary Table 1). The individuals, relative to other ni-Vanuatu, which suggests gene flow final dataset involves 462 unrelated individuals, including 355 individu- from Polynesia6,23. als from the Pacific region, and 35,870,981 single-nucleotide