Demographic history and genetic structure in pre-Hispanic Central Mexico

Aridoamerica and Mesoamerica are two distinct cultural areas that hosted numerous pre-Hispanic civilizations between 2,500 BCE and 1,521 CE. The division between these regions shifted southward due to severe droughts ca. 1,100 years ago, allegedly driving demographic changes and population replacement in some sites in central Mexico. Here, we present shotgun genome-wide data from 12 individuals and 26 mitochondrial genomes from eight pre-Hispanic archaeological sites across Mexico, including two at the shifting border of Aridoamerica and Mesoamerica. We find population continuity spanning the climate change episode and a broad preservation of the genetic structure across present-day Mexico for the last 2,300 years. Lastly, we identify a contribution to pre-Hispanic populations of northern and central Mexico from an ancient unsampled ‘ghost’ population.

[1]  Deborah A. Bolnick,et al.  The genomic landscape of Mexican Indigenous populations brings insights into the peopling of the Americas , 2021, Nature Communications.

[2]  J. Novembre,et al.  Parental relatedness through time revealed by runs of homozygosity in ancient DNA , 2021, Nature Communications.

[3]  Natalie M. Myres,et al.  The Mitochondrial DNA Landscape of Modern Mexico , 2021, Genes.

[4]  O. François,et al.  Factor analysis of ancient population genomic samples , 2020, Nature Communications.

[5]  Swapan Mallick,et al.  Insights into human genetic variation and population history from 929 diverse genomes , 2019, Science.

[6]  N. Nowaczyk,et al.  High resolution paleoclimate and paleoenvironmental reconstruction in the Northern Mesoamerican Frontier for Prehistory to Historical times , 2019 .

[7]  C. Bustamante,et al.  Ancient DNA reconstructs the genetic legacies of pre-contact Puerto Rico communities , 2019, bioRxiv.

[8]  P. Visscher,et al.  Extreme inbreeding in a European ancestry sample from the contemporary UK population , 2019, Nature Communications.

[9]  Christopher R. Gignoux,et al.  Population History and Gene Divergence in Native Mexicans Inferred from 76 Human Exomes , 2019, bioRxiv.

[10]  C. Speller,et al.  Ancient mitochondrial DNA and population dynamics in postclassic Central Mexico: Tlatelolco (ad 1325–1520) and Cholula (ad 900–1350) , 2019, Archaeological and Anthropological Sciences.

[11]  Yun S. Song,et al.  Early human dispersals within the Americas , 2018, Science.

[12]  A. Muñoz,et al.  Un minero en la Sierra Gorda: caso de contaminación ocupacional multielemental de metales pesados a finales del periodo Clásico , 2018 .

[13]  Kelly M. Harkins,et al.  Reconstructing the Deep Population History of Central and South America , 2018, Cell.

[14]  Luca Pagani,et al.  Ancient human parallel lineages within North America contributed to a coastal expansion , 2018, Science.

[15]  C. Bustamante,et al.  Genomic insights into the origin and diversification of late maritime hunter-gatherers from the Chilean Patagonia , 2018, Proceedings of the National Academy of Sciences.

[16]  C. Bustamante,et al.  Ancient genomes from North Africa evidence prehistoric migrations to the Maghreb from both the Levant and Europe , 2018, Proceedings of the National Academy of Sciences.

[17]  Peter K. Joshi,et al.  Runs of homozygosity: windows into population history and trait architecture , 2018, Nature Reviews Genetics.

[18]  John A. Kamm,et al.  Terminal Pleistocene Alaskan genome reveals first founding population of Native Americans , 2018, Nature.

[19]  J. Fernández-López,et al.  Demographic history and biologically relevant genetic variation of Native Mexicans inferred from whole-genome sequencing , 2017, Nature Communications.

[20]  J. Schraiber Assessing the Relationship of Ancient and Modern Populations , 2017, Genetics.

[21]  Daniel Wegmann,et al.  ATLAS: Analysis Tools for Low-depth and Ancient Samples , 2017, bioRxiv.

[22]  M. Jakobsson,et al.  Estimating genetic kin relationships in prehistoric populations , 2017, bioRxiv.

[23]  Yun S. Song,et al.  The Simons Genome Diversity Project: 300 genomes from 142 diverse populations , 2016, Nature.

[24]  Maria Cerezo,et al.  Punctuated bursts in human male demography inferred from 1,244 worldwide Y-chromosome sequences , 2016, Nature Genetics.

[25]  Hans-Jürgen Bandelt,et al.  HaploGrep 2: mitochondrial haplogroup classification in the era of high-throughput sequencing , 2016, Nucleic Acids Res..

[26]  Cristina E. Valdiosera,et al.  Ancient mitochondrial DNA provides high-resolution time scale of the peopling of the Americas , 2016, Science Advances.

[27]  R. J. Herrera,et al.  Mayans: a Y chromosome perspective , 2016, European Journal of Human Genetics.

[28]  Julie A. Hoggarth,et al.  The political collapse of Chichén Itzá in climatic and cultural context , 2016 .

[29]  Stinus Lindgreen,et al.  AdapterRemoval v2: rapid adapter trimming, identification, and read merging , 2016, BMC Research Notes.

[30]  I. Silva-Zolezzi,et al.  Genetic Diversity and Differentiation in Urban and Indigenous Populations of Mexico: Patterns of Mitochondrial DNA and Y-Chromosome Lineages , 2016, Biodemography and social biology.

[31]  Sohini Ramachandran,et al.  pong: fast analysis and visualization of latent clusters in population genetic data , 2015, bioRxiv.

[32]  Mannis van Oven,et al.  PhyloTree Build 17: Growing the human mitochondrial DNA tree , 2015 .

[33]  Janet Kelso,et al.  Schmutzi: estimation of contamination and endogenous mitochondrial consensus calling for ancient DNA , 2015, Genome Biology.

[34]  Dafne Angélica Corona Velázquez Expansión Territorial Comercial en Mesoamérica y Mesoamérica Septentrional por Medio del Intercambio , 2015 .

[35]  David Bryant,et al.  popart: full‐feature software for haplotype network construction , 2015 .

[36]  Mattias Jakobsson,et al.  Genomic evidence for the Pleistocene and recent population history of Native Americans , 2015, Science.

[37]  R. Montiel,et al.  Genetic Evidence Supports the Multiethnic Character of Teopancazco, a Neighborhood Center of Teotihuacan, Mexico (AD 200-600) , 2015, PloS one.

[38]  Swapan Mallick,et al.  An early modern human from Romania with a recent Neanderthal ancestor , 2015, Nature.

[39]  Christopher R. Gignoux,et al.  The genetics of Mexico recapitulates Native American substructure and affects biomedical traits , 2014, Science.

[40]  Dong Xie,et al.  BEAST 2: A Software Platform for Bayesian Evolutionary Analysis , 2014, PLoS Comput. Biol..

[41]  Mattias Jakobsson,et al.  The genome of a Late Pleistocene human from a Clovis burial site in western Montana , 2014, Nature.

[42]  M. Jakobsson,et al.  Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal , 2014, Proceedings of the National Academy of Sciences.

[43]  M. Jakobsson,et al.  Accurate sex identification of ancient human remains using DNA shotgun sequencing , 2013 .

[44]  Cristina E. Valdiosera,et al.  Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments , 2013, Proceedings of the National Academy of Sciences.

[45]  R. J. Herrera,et al.  Reconciling migration models to the Americas with the variation of North American native mitogenomes , 2013, Proceedings of the National Academy of Sciences.

[46]  Philip L. F. Johnson,et al.  mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters , 2013, Bioinform..

[47]  Timothy Daley,et al.  Predicting the molecular complexity of sequencing libraries , 2013, Nature Methods.

[48]  Swapan Mallick,et al.  Ancient Admixture in Human History , 2012, Genetics.

[49]  H. Rangel-Villalobos,et al.  Reconstructing the History of Mesoamerican Populations through the Study of the Mitochondrial DNA Control Region , 2012, PloS one.

[50]  Richard M Myers,et al.  Genomic patterns of homozygosity in worldwide human populations. , 2012, American journal of human genetics.

[51]  P. Underhill,et al.  Y-chromosome diversity in Native Mexicans reveals continental transition of genetic structure in the Americas. , 2012, American journal of physical anthropology.

[52]  Brendan D. O'Fallon,et al.  Native Americans experienced a strong population bottleneck coincident with European contact , 2011, Proceedings of the National Academy of Sciences.

[53]  R. Testa,et al.  Mitochondrial DNA Backgrounds Might Modulate Diabetes Complications Rather than T2DM as a Whole , 2011, PloS one.

[54]  Harry Campbell,et al.  Genomic Runs of Homozygosity Record Population History and Consanguinity , 2010, PloS one.

[55]  Natalie M. Myres,et al.  The initial peopling of the Americas: a growing number of founding mitochondrial genomes from Beringia. , 2010, Genome research.

[56]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[57]  Matthias Meyer,et al.  Illumina sequencing library preparation for highly multiplexed target capture and sequencing. , 2010, Cold Spring Harbor protocols.

[58]  R. Malhi,et al.  Evaluating the Farming/Language Dispersal Hypothesis with genetic variation exhibited by populations in the Southwest and Mesoamerica , 2010, Proceedings of the National Academy of Sciences.

[59]  A. Krogh,et al.  Ancient human genome sequence of an extinct Palaeo-Eskimo , 2010, Nature.

[60]  S. Macfarlan,et al.  Inferring Relationships Between Indigenous Baja California Sur and Seri/Comcáac Populations Through Cultural Traits , 2010 .

[61]  David H. Alexander,et al.  Fast model-based estimation of ancestry in unrelated individuals. , 2009, Genome research.

[62]  Manfred Kayser,et al.  Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation , 2009, Human mutation.

[63]  Natalie M. Myres,et al.  Distinctive Paleo-Indian Migration Routes from Beringia Marked by Two Rare mtDNA Haplogroups , 2009, Current Biology.

[64]  Lahiri Kanth Nanduri,et al.  Validation of microarray‐based resequencing of 93 worldwide mitochondrial genomes , 2009, Human mutation.

[65]  A. Drummond,et al.  Bayesian inference of population size history from multiple loci , 2008, BMC Evolutionary Biology.

[66]  Igor Rudan,et al.  Runs of homozygosity in European populations. , 2008, American journal of human genetics.

[67]  David Reich,et al.  Principal component analysis of genetic data , 2008, Nature Genetics.

[68]  J. Stephenson 1000 Genomes Project , 2008 .

[69]  M. D. Mayor,et al.  Sex Identification of Children Sacrificed to the Ancient Aztec Rain Gods in Tlatelolco , 2008 .

[70]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[71]  Michael Hofreiter,et al.  Ancient DNA extraction from bones and teeth , 2007, Nature Protocols.

[72]  D. Reich,et al.  Population Structure and Eigenanalysis , 2006, PLoS genetics.

[73]  David W. Stahle,et al.  Megadrought and Megadeath in 16th Century Mexico , 2002, Emerging infectious diseases.

[74]  S. Pääbo,et al.  Mitochondrial genome variation and the origin of modern humans , 2000, Nature.

[75]  S. O'Hara,et al.  On the arid margin: the relationship between climate, humans and the environment. A review of evidence from the highlands of central Mexico. , 1994, Chemosphere.

[76]  Malcolm K. Hughes,et al.  Was there a ‘medieval warm period’, and if so, where and when? , 1994 .

[77]  B. Braniff Oscilación de la frontera norte mesoamericana: un nuevo ensayo , 1989 .

[78]  G. Kubler The Population of Central Mexico in the Sixteenth Century , 1978 .

[79]  B. Bainbridge,et al.  Genetics , 1981, Experientia.

[80]  Francisco Javier Clavijero Historia antigua de México , 1958 .