. 2020 May 28;181(5):1131-1145.e21.

doi: 10.1016/j.cell.2020.04.015. Epub 2020 May 7.

A Paleogenomic Reconstruction of the Deep Population History of the Andes

Nathan Nakatsuka¹, Iosif Lazaridis², Chiara Barbieri³, Pontus Skoglund⁴, Nadin Rohland², Swapan Mallick⁵, Cosimo Posth⁶, Kelly Harkins-Kinkaid⁷, Matthew Ferry⁸, Éadaoin Harney⁸, Megan Michel⁸, Kristin Stewardson⁸, Jannine Novak-Forst⁷, José M Capriles⁹, Marta Alfonso Durruty¹⁰, Karina Aranda Álvarez¹¹, David Beresford-Jones¹², Richard Burger¹³, Lauren Cadwallader¹⁴, Ricardo Fujita¹⁵, Johny Isla¹⁶, George Lau¹⁷, Carlos Lémuz Aguirre¹⁸, Steven LeBlanc¹⁹, Sergio Calla Maldonado¹⁸, Frank Meddens²⁰, Pablo G Messineo²¹, Brendan J Culleton²², Thomas K Harper⁹, Jeffrey Quilter¹⁹, Gustavo Politis²¹, Kurt Rademaker²³, Markus Reindel²⁴, Mario Rivera²⁵, Lucy Salazar¹², José R Sandoval¹⁵, Calogero M Santoro²⁶, Nahuel Scheifler²¹, Vivien Standen²⁷, Maria Ines Barreto²⁸, Isabel Flores Espinoza²⁸, Elsa Tomasto-Cagigao²⁹, Guido Valverde³⁰, Douglas J Kennett³¹, Alan Cooper³⁰, Johannes Krause⁶, Wolfgang Haak⁶, Bastien Llamas³⁰, David Reich³², Lars Fehren-Schmitz³³

Affiliations

¹ Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Harvard-MIT Division of Health Sciences and Technology, Boston, MA 02115, USA. Electronic address: nathan_nakatsuka@hms.harvard.edu.
² Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA.
³ Max Planck Institute for the Science of Human History, Jena 07745, Germany; Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich 8057, Switzerland.
⁴ Francis Crick Institute, London NW1 1AT, UK.
⁵ Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02446, USA; Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA.
⁶ Max Planck Institute for the Science of Human History, Jena 07745, Germany.
⁷ UCSC Paleogenomics, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.
⁸ Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02446, USA.
⁹ Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA.
¹⁰ Department of Sociology, Anthropology and Social Work, Kansas State University, Manhattan, KS 66506, USA.
¹¹ Sociedad de Arqueología de La Paz, 5294 La Paz, Bolivia.
¹² McDonald Institute for Archaeological Research, University of Cambridge, Downing St., Cambridge, CB2 3ER, UK.
¹³ Department of Anthropology, Yale University, New Haven, CT 06511, USA.
¹⁴ Office of Scholarly Communication, Cambridge University Library, Cambridge CB3 9DR, UK.
¹⁵ Centro de Genética y Biología Molecular, Facultdad de Medicina, Universidad de San Martín de Porres, Lima 15011, Peru.
¹⁶ Peruvian Ministry of Culture, DDC Ica, Directos of the Nasca-Palpa Management Plan, Calle Juan Matta 880, Nasca 11401, Peru.
¹⁷ Sainsbury Research Unit, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK.
¹⁸ Carrera de Arqueología, Universidad Mayor de San Andrés, Edificio Facultad de Ciencias Sociales 3er Piso, La Paz 1995, Bolivia.
¹⁹ Harvard Peabody Museum, Harvard University, Cambridge, MA 02138, USA.
²⁰ School of Archaeology, Geography and Environmental Sciences, University of Reading, Reading, Berkshire, RG6 6AH, UK.
²¹ INCUAPA-CONICET, Facultad de Ciencias Sociales, Universidad Nacional del Centro de la Provincia de Buenos Aires, Olavarría 7400, Argentina.
²² Institutes for Energy and the Environment, The Pennsylvania State University, University Park, PA 16802, USA.
²³ Department of Anthropology, Michigan State University, East Lansing, MI 48824, USA.
²⁴ Commission for Archaeology of Non-European Cultures, German Archaeological Institute, Berlin 14195, Germany.
²⁵ Universidad de Magallanes, Punta Arenas 6210427, Chile; Field Museum Natural History 1400 S Lake Shore Dr., Chicago, IL 60605, USA.
²⁶ Instituto de Alta Investigation, Universidad de Tarapaca, Antafogasta 1520, Arica, 1000000, Chile.
²⁷ Departamento de Antropología, Universidad de Tarapacá, Antafogasta 1520, Arica, 1000000, Chile.
²⁸ Museo de Sitio Huaca Pucllana, Calle General Borgoño, Cuadra 8, Miraflores, Lima 18, Peru.
²⁹ Department of Humanities, Pontifical Catholic University of Peru, San Miguel 15088, Peru.
³⁰ Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, Adelaide University, Adelaide, SA 5005, Australia.
³¹ Institutes for Energy and the Environment, The Pennsylvania State University, University Park, PA 16802, USA; Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA; Department of Anthropology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA.
³² Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02446, USA; Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA; Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. Electronic address: reich@genetics.med.harvard.edu.
³³ UCSC Paleogenomics, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; UCSC Genomics Institute, University of California, Santa Cruz, Santa Cruz, CA 95064, USA. Electronic address: lfehrens@ucsc.edu.

PMID: 32386546
PMCID: PMC7304944
DOI: 10.1016/j.cell.2020.04.015

A Paleogenomic Reconstruction of the Deep Population History of the Andes

Nathan Nakatsuka et al. Cell. 2020.

. 2020 May 28;181(5):1131-1145.e21.

doi: 10.1016/j.cell.2020.04.015. Epub 2020 May 7.

Authors

Affiliations

¹ Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Harvard-MIT Division of Health Sciences and Technology, Boston, MA 02115, USA. Electronic address: nathan_nakatsuka@hms.harvard.edu.
² Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA.
³ Max Planck Institute for the Science of Human History, Jena 07745, Germany; Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich 8057, Switzerland.
⁴ Francis Crick Institute, London NW1 1AT, UK.
⁵ Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02446, USA; Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA.
⁶ Max Planck Institute for the Science of Human History, Jena 07745, Germany.
⁷ UCSC Paleogenomics, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.
⁸ Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02446, USA.
⁹ Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA.
¹⁰ Department of Sociology, Anthropology and Social Work, Kansas State University, Manhattan, KS 66506, USA.
¹¹ Sociedad de Arqueología de La Paz, 5294 La Paz, Bolivia.
¹² McDonald Institute for Archaeological Research, University of Cambridge, Downing St., Cambridge, CB2 3ER, UK.
¹³ Department of Anthropology, Yale University, New Haven, CT 06511, USA.
¹⁴ Office of Scholarly Communication, Cambridge University Library, Cambridge CB3 9DR, UK.
¹⁵ Centro de Genética y Biología Molecular, Facultdad de Medicina, Universidad de San Martín de Porres, Lima 15011, Peru.
¹⁶ Peruvian Ministry of Culture, DDC Ica, Directos of the Nasca-Palpa Management Plan, Calle Juan Matta 880, Nasca 11401, Peru.
¹⁷ Sainsbury Research Unit, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK.
¹⁸ Carrera de Arqueología, Universidad Mayor de San Andrés, Edificio Facultad de Ciencias Sociales 3er Piso, La Paz 1995, Bolivia.
¹⁹ Harvard Peabody Museum, Harvard University, Cambridge, MA 02138, USA.
²⁰ School of Archaeology, Geography and Environmental Sciences, University of Reading, Reading, Berkshire, RG6 6AH, UK.
²¹ INCUAPA-CONICET, Facultad de Ciencias Sociales, Universidad Nacional del Centro de la Provincia de Buenos Aires, Olavarría 7400, Argentina.
²² Institutes for Energy and the Environment, The Pennsylvania State University, University Park, PA 16802, USA.
²³ Department of Anthropology, Michigan State University, East Lansing, MI 48824, USA.
²⁴ Commission for Archaeology of Non-European Cultures, German Archaeological Institute, Berlin 14195, Germany.
²⁵ Universidad de Magallanes, Punta Arenas 6210427, Chile; Field Museum Natural History 1400 S Lake Shore Dr., Chicago, IL 60605, USA.
²⁶ Instituto de Alta Investigation, Universidad de Tarapaca, Antafogasta 1520, Arica, 1000000, Chile.
²⁷ Departamento de Antropología, Universidad de Tarapacá, Antafogasta 1520, Arica, 1000000, Chile.
²⁸ Museo de Sitio Huaca Pucllana, Calle General Borgoño, Cuadra 8, Miraflores, Lima 18, Peru.
²⁹ Department of Humanities, Pontifical Catholic University of Peru, San Miguel 15088, Peru.
³⁰ Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, Adelaide University, Adelaide, SA 5005, Australia.
³¹ Institutes for Energy and the Environment, The Pennsylvania State University, University Park, PA 16802, USA; Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA; Department of Anthropology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA.
³² Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02446, USA; Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA; Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. Electronic address: reich@genetics.med.harvard.edu.
³³ UCSC Paleogenomics, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; UCSC Genomics Institute, University of California, Santa Cruz, Santa Cruz, CA 95064, USA. Electronic address: lfehrens@ucsc.edu.

PMID: 32386546
PMCID: PMC7304944
DOI: 10.1016/j.cell.2020.04.015

Abstract

There are many unanswered questions about the population history of the Central and South Central Andes, particularly regarding the impact of large-scale societies, such as the Moche, Wari, Tiwanaku, and Inca. We assembled genome-wide data on 89 individuals dating from ∼9,000-500 years ago (BP), with a particular focus on the period of the rise and fall of state societies. Today's genetic structure began to develop by 5,800 BP, followed by bi-directional gene flow between the North and South Highlands, and between the Highlands and Coast. We detect minimal admixture among neighboring groups between ∼2,000-500 BP, although we do detect cosmopolitanism (people of diverse ancestries living side-by-side) in the heartlands of the Tiwanaku and Inca polities. We also highlight cases of long-range mobility connecting the Andes to Argentina and the Northwest Andes to the Amazon Basin. VIDEO ABSTRACT.

Keywords: Andes; ancient DNA; anthropology; archaeology; population genetics.

PubMed Disclaimer

Conflict of interest statement

Declaration of Interests The authors declare no competing interests.

Figures

**Figure 1**
Distribution of Pre-Hispanic Individuals Over Space and Time (A) Map with the locations of 86 ancient individuals (3 from our study are not included here due to very low coverage). Dotted lines represent regions defined for this study. Highland individuals are triangles and Coast individuals are circles. Coloring corresponds to genetic profiles, which in most cases match the geographic regions. (B) Groupings of ancient individuals based on geography and archaeological period (Table S1). Italics indicate previously published individuals, and sample sizes are in parentheses (yellow indicates shotgun sequences). Map was made with Natural Earth.

**Figure S1**
Images of Archaeological Sites, Related to STAR Methods (A) Location of Pukara in the Altiplano of northern Chile and South America (https://satellites.pro/mapa_de_Chile#-17.801972,-69.317661,19). (B) Undisturbed stone funerary cist of Pukara 3, close to the border of the cliff above Pukara 1. (C) Cist 1 and 2 (left to right) of Pukara 6. Disturbed and badly preserved human remains for this study come from cist or Tomb 1 (60 cm height, less than one m in diameter). The cists are surrounded by *tola* vegetation. (D) Iroco site (Bolivia). (E) Tiwanaku burial (Locus 785). (F) Tiwanaku cist tomb (Locus 719) with the sample individual 5 (MIS5). (G) Fragment of keru with the representation of the “staffed god.”

**Figure S2**
Mitochondrial DNA Tree, Related to Figures 3 and 4 Phylogenetic tree built with maximum parsimony algorithm of 136 ancient mtDNA (newly reconstructed sequences in red and previously published sequences in blue) and 197 modern mtDNA sequences (in black font) built using MEGA6 (Tamura et al., 2013) with an African mtDNA sequence used to root the tree (not shown). (A) Tree section including mtDNA haplogroups C1, D4h3a and D1. (B) Tree section including mtDNA haplogroup A2 and B2. Related to Table S1.

**Figure S3**
ADMIXTURE Plot at Different K Values, Related to Figure 2 The run with the highest log-likelihood score after 100 trials was taken for each K value.

**Figure 2**
Principal Components Analysis (PCA) of Ancient Individuals Projected onto Modern Variation from Labeled Groups Modern individuals are in gray, and ancient individuals form a gradient that correlates to latitude (coloring is directly based on latitude with blue most north and red most south; numbers are latitude degrees). We removed 16 outliers from North Chile, Cusco, and Argentina that have evidence of ancestry from gene flows outside each region, and *Peru_Lauricocha_8600BP* and *Peru_Cuncaicha_9000BP*, which were too old to share the latitudinal cline (Figure S4 includes them). The percentage of total variation explained by each PC is shown in parentheses on each axis.

**Figure S4**
PCA of Additional Samples Removed from Figure 2, Related to Figure 2 Principal Components Analysis (PCA) of ancient samples projected onto modern individuals from the Andes and Amazon region (Barbieri et al., 2019). Eigenvector 1 coordinates were reversed so that the PCA correlates with geographical structure. Ancient individuals of Figure 2 are shown on a blue-red latitudinal gradient. Modern individuals are in gray. In black are all individuals that we removed from Figure 2 due to their outlier status reflecting distinctive histories that we discuss in the text (*NorthChile* individuals, Cusco individuals, the Argentinian Inca individual, and the *Peru_Lauricocha_8600BP* and *Peru_Cuncaicha_9000BP* individuals). The percentage of total variation explained by each PC is shown in parentheses on each axis.

**Figure 3**
Neighbor-Joining Tree Based on Inverted Outgroup-f₃ Statistics (1/f₃(*Mbuti*; *Group1*, *Group2*)) Only individuals with >40,000 SNPs are included.

**Figure S5**
Multi-Dimensional Scaling (MDS) Plot of the Matrix of Statistics of the Form 1-f₃(*Mbuti*; *South American 1*, *South American 2*), Related to Figure 2 Only individuals with > 100,000 SNPs are included. (A) Plot of all groups. (B) Plot of all groups younger than ~5900 BP, with the outliers *Peru_Lauricocha_3600BP* and *Peru_Cuncaicha_3300BP* removed. (C) Plot of all Andean groups younger than ~3000 BP.

**Figure S6**
Admixture Graphs Generated through a Semi-Automated Process, Related to Figures 3 and 4 and Table S1 (A) This is the best fitting graph relating these groups (maximum |Z-score| = 2.5). Mixtures between South Peru Highlands (*Peru_Cuncaicha_4200BP*) and North Peru Highlands (*Peru_Lauricocha_5800BP* and *Peru_LaGalgada_4100BP*) were required in all fitting graphs (maximum |Z| < 3). (B) Admixture graph modeling Amazonian ancestry (related to *Peru_SanMartin_modern*) in *NorthPeruCoast*, *NorthPeruHighlands*, and *CentralPeruCoast*. Maximum |Z-score| = 3.0. (C) Admixture graph that fits the data (maximum |Z-score| = 3.1), showing *Argentina_LagunaChica_1600BP* as admixed from a population related to *Argentina_LagunaChica_6800BP* and *NorthChile*.

**Figure S7**
Heatmap of Outgroup f₃-Statistics, Related to Figure 2 Color coding is based on statistics of the form f₃(Mbuti; Ancient, Modern), where the Ancient groups are (A) Peru_SouthHighlands_Cuncaicha_9000BP, (B) Peru_NorthHighlands_Lauricocha_8600BP, (C) Peru_NorthHighlands_Lauricocha_5800BP, (D) Peru_SouthHighlands_Cuncaicha_4200BP, (E) Peru_NorthHighlands_LaGalgada_4100BP, (F) NorthPeruCoast, (G) NorthPeruHighlands, (H) CentralPeruCoast, (I) SouthPeruCoast, (J) SouthPeruHighlands, (K) NorthChile, (L) Peru_TiticacaBasin_RioUncallane_1700BP, (M) Bolivia_TiticacaBasin_Tiwanaku_1000BP, and (N) Peru_Cusco_SanSebastian_610-490BP. Modern groups are from Barbieri et al. (2019). Related to Table S6.

**Figure 4**
Overview of Findings Admixture graph fit (maximum |Z| score between observed and expected f-statistics is 3.1). *Chile_Pica8_700BP* was removed from *NorthChile* due to low coverage.

**Figure S8**
*qpWave* Analyses, Related to STAR Methods *qpWave* analyses with all pairs (Pairs_Rank0) or triplets (Triplets_Rank0 or Triplets_Rank1) of all Andean and North Chile groups when compared with *Peru_Lauricocha_8600BP*. Rank 0 and 1 refers to a model in which all populations in the analysis fit as derived from one or two ancestral populations, respectively, relative to the outgroups (rejection of these ranks means that additional sources of ancestry are required to model the populations). Modern groups and shotgun samples were excluded due to potential for artifacts. *Peru_Lauricocha_5800BP* and *Peru_Lauricocha_3600BP* were also excluded due to their previously known lack of California Channel Island-related ancestry (Posth et al., 2018). Color-coding refers to pairs or triples that include groups that consistently do not fit in some two-source or three-source models: the Cuncaicha 3300 BP and 4200 BP individuals are the only groups that are consistently poorly modeled even without a third source of ancestry. Related to Table S8.

**Figure 5**
Map Summarizing Genetic Exchanges in the Central Andes (1) Bi-directional mixture between the North and Central Coasts and the Northwest Amazon. (2) Genetic exchange between *NorthPeruCoast* and *NorthPeruHighlands*. (3) Genetic interaction between *CentralPeruCoast* and *NorthPeruHighlands_Lauricocha* before ~5800 BP. (4) Genetic exchange between *NorthPeruHighlands* and *SouthPeruHighlands*. (5) Individuals of *NorthPeruCoast* and Titicaca Basin-related ancestry found in Cusco (Torontoy) during the Inca Empire (~450 BP). (6) Spread of *SouthPeruHighlands-*related ancestry into the Cusco region 450 BP–present. (7) Genetic exchange between *SouthPeruHighlands* and Titicaca Basin before 1,700 BP. (8) Greater allele sharing between Tiwanaku and *SouthPeruHighlands* relative to other individuals in Titicaca Basin during the Tiwanaku period (~1,000 BP). (9) *SouthPeruHighlands*-related ancestry found in Pukara in Northern Chile ~700 BP. (10) Genetic exchange between *NorthChile* and Titicaca Basin before ~1,700 BP. (11) *NorthPeruCoast*-related ancestry found in an Inca sacrifice victim in Argentina. (12) Gene flow between *NorthChile* or *SouthPeruHighlands* and the Pampas region of Argentina.

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References

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A Paleogenomic Reconstruction of the Deep Population History of the Andes

Affiliations

A Paleogenomic Reconstruction of the Deep Population History of the Andes

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources