Inca and Spanish Empires had a profound impact on Peruvian demography

peru-population-history

Open access Evolutionary genomic dynamics of Peruvians before, during, and after the Inca Empire by Harris et al., PNAS (2018) 201720798 (published ahead of print).

Abstract (emphasis mine):

Native Americans from the Amazon, Andes, and coastal geographic regions of South America have a rich cultural heritage but are genetically understudied, therefore leading to gaps in our knowledge of their genomic architecture and demographic history. In this study, we sequence 150 genomes to high coverage combined with an additional 130 genotype array samples from Native American and mestizo populations in Peru. The majority of our samples possess greater than 90% Native American ancestry, which makes this the most extensive Native American sequencing project to date. Demographic modeling reveals that the peopling of Peru began ∼12,000 y ago, consistent with the hypothesis of the rapid peopling of the Americas and Peruvian archeological data. We find that the Native American populations possess distinct ancestral divisions, whereas the mestizo groups were admixtures of multiple Native American communities that occurred before and during the Inca Empire and Spanish rule. In addition, the mestizo communities also show Spanish introgression largely following Peruvian Independence, nearly 300 y after Spain conquered Peru. Further, we estimate migration events between Peruvian populations from all three geographic regions with the majority of between-region migration moving from the high Andes to the low-altitude Amazon and coast. As such, we present a detailed model of the evolutionary dynamics which impacted the genomes of modern-day Peruvians and a Native American ancestry dataset that will serve as a beneficial resource to addressing the underrepresentation of Native American ancestry in sequencing studies.

peru-admixture
Admixture among Peruvian populations. (A) Colors represent contributions from donor populations into the genomes of Peruvian mestizo groups, as estimated by CHROMOPAINTER and GLOBETROTTER. The label within parentheses for each Peruvian Native American source population corresponds to their geographic region where Ama, And, and Coa represent Amazon, Andes, and coast, respectively. (B) Admixture time and proportion for the best fit three-way ancestry (AP, Trujillo and Lima) and two-way ancestry (Iquitos, Cusco, and Puno) TRACT models [European, African, and Native American (NatAm) ancestries] for six mestizo populations. (C) Network of individuals from Peruvian Native American and mestizo groups according to their shared IBD length. Each node is an individual and the length of an edge equals to (1/total shared IBD). IBD segments with different lengths are summed according to different thresholds representing different times in the past (52), with 7.8 cM, 9.3 cM, and 21.8 cM roughly representing the start of the Inca Empire, the Spanish conquest and occupation, and Peruvian independence. IBD networks are generated by Cytoscape (98) and only the major clusters in the network are shown for different cutoffs of segment length. AP, Central Am, and Matsig are short for Afroperuvians, Central American, and Matsiguenka, respectively. The header of each IBD network specifies the length of IBD segments used in each network.

Interesting excerpts

The high frequency of Native American mitochondrial haplotypes suggests that European males were the primary source of European admixture with Native Americans, as previously found (23, 24, 41, 42). The only Peruvian populations that have a proportion of the Central American component are in the Amazon (Fig. 2A). This is supported by Homburger et al. (4), who also found Central American admixture in other Amazonian populations and could represent ancient shared ancestry or a recent migration between Central America and the Amazon.

Following the peopling of Peru, we find a complex history of admixture between Native American populations from multiple geographic regions (Figs. 2B and 3 A and C). This likely began before the Inca Empire due to Native American and mestizo groups sharing IBD segments that correspond to the time before the Inca Empire. However, the Inca Empire likely influenced this pattern due to their policy of forced migrations, known as “mitma” (mitmay in Quechua) (28, 31, 37), which moved large numbers of individuals to incorporate them into the Inca Empire. We can clearly see the influence of the Inca through IBD sharing where the center of dominance in Peru is in the Andes during the Inca Empire (Fig. 3C).

peru-population-pca
ASPCA of combined Peruvian Genome Project with the HGDP genotyped on the Human Origins Array. A.) European ancestry. B.) African ancestry. Samples are filtered by their corresponding ancestral proportion: European ≥ 30% (panel A) and African ≥ 10% (panel B). The two plots in each panel are identical except for the color scheme: reference populations are colored on the left and Peruvian populations are colored on the right. Each point is one haplotype. In the African ASPCA we note three outliers among our samples, two from Trujillo and one from Iquitos, that cluster closer to the Luhya and Luo populations, though not directly. It is likely that these individuals share ancestry with other regions of Africa in addition to western Africa, but we cannot test this hypothesis explicitly as we have too few samples.

A similar policy of large-scale consolidation of multiple Native American populations was continued during Spanish rule through their program of reducciones, or reductions (31, 32), which is consistent with the hypothesis that the Inca and Spanish had a profound impact on Peruvian demography (25). The result of these movements of people created early New World cosmopolitan communities with genetic diversity from the Andes, Amazon, and coast regions as is evidenced by mestizo populations’ ancestry proportions (Fig. 3A). Following Peruvian independence, these cosmopolitan populations were those same ones that predominantly admixed with the Spanish (Fig. 3B). Therefore, this supports our model that the Inca Empire and Spanish colonial rule created these diverse populations as a result of admixture between multiple Native American ancestries, which would then go on to become the modern mestizo populations by admixing with the Spanish after Peruvian independence.

Further, it is interesting that this admixture began before the urbanization of Peru (26) because others suspected the urbanization process would greatly impact the ancestry patterns in these urban centers (25). (…)

Related

Native American genetic continuity and oldest mtDNA hg A2ah in the Andean region

Native American gene continuity to the modern admixed population from the Colombian Andes: Implication for biomedical, population and forensic studies by Criollo-Rayo et al., Forensic Sci Int Genet (2018), in press, corrected proof.

Abstract (emphasis mine):

Andean populations have variable degrees of Native American and European ancestry, representing an opportunity to study admixture dynamics in the populations from Latin America (also known as Hispanics). We characterized the genetic structure of two indigenous (Nasa and Pijao) and three admixed (Ibagué, Ortega and Planadas) groups from Tolima, in the Colombian Andes. DNA samples from 348 individuals were genotyped for six mitochondrial DNA (mtDNA), seven non-recombining Y-chromosome (NRY) region and 100 autosomal ancestry informative markers. Nasa and Pijao had a predominant Native American ancestry at the autosomal (92%), maternal (97%) and paternal (70%) level. The admixed groups had a predominant Native American mtDNA ancestry (90%), a substantial frequency of European NRY haplotypes (72%) and similar autosomal contributions from Europeans (51%) and Amerindians (45%). Pijao and nearby Ortega were indistinguishable at the mtDNA and autosomal level, suggesting a genetic continuity between them. Comparisons with multiple Native American populations throughout the Americas revealed that Pijao, had close similarities with Carib-speakers from distant parts of the continent, suggesting an ancient correlation between language and genes. In summary, our study aimed to understand Hispanic patterns of migration, settlement and admixture, supporting an extensive contribution of local Amerindian women to the gene pool of admixed groups and consistent with previous reports of European-male driven admixture in Colombia.

andean-y-dna-mtdna
Ancestral uniparental haplogroups and diversity in Tolima. Geography of sampling locations. The
top and middle sections show the frequency of Native American mtDNA haplogroups and NRY lineages for all
populations. Gene diversity is shown below their respective pie chart. The lower part depicts the geography of the
region where the sampling sites of Ortega and Pijao are closely located in Tolima’s Magdalena river valley and
Ibague, Planadas and Nasa located in the Andes cordilleras (additional geographic details are shown in SF1).

Highlights from the paper:

  • MtDNA suggest a pre/post Columbian genetic continuity in the Colombian Andes.
  • Y-chromosome diversity follows a clinal gradient in the studied region.
  • Sex-biased/male-driven admixture process, involving Pijao women with European men.
  • Admixed closer to Indigenous resguardos have a higher Native American ancestry.

Also interesting is the recent paper Mitochondrial lineage A2ah found in a pre‐Hispanic individual from the Andean region, by Russo et al., in American Journal of Human Biology (2018), with an interesting sample from the Regional Developments II period (540 ± 60 BP).

phylogeny-a2ah-mtdna
Phylogeny of the A2ah mitochondrial lineage based on HVR I sequences. Both MaximumParsimony andMaximumLikelihood reconstructions led to the same typology. The tree was rooted with the RSRS. Sample ID: Cueva: Pukara de La Cueva, STACRUZ: Santa Cruz, BNI: Beni, BR: South-eastern Brazil, TobaChA: TobaGranChaco

Related:

Ancient Patagonian genomes suggest origin and diversification of late maritime hunter-gatherers

ancient-patagonia-admixture

Genomic insights into the origin and diversification of late maritime hunter-gatherers from the Chilean Patagonia, by de la Fuente et al. PNAS (2018) published ahead of print.

Abstract (emphasis mine):

Patagonia was the last region of the Americas reached by humans who entered the continent from Siberia ∼15,000–20,000 y ago. Despite recent genomic approaches to reconstruct the continental evolutionary history, regional characterization of ancient and modern genomes remains understudied. Exploring the genomic diversity within Patagonia is not just a valuable strategy to gain a better understanding of the history and diversification of human populations in the southernmost tip of the Americas, but it would also improve the representation of Native American diversity in global databases of human variation. Here, we present genome data from four modern populations from Central Southern Chile and Patagonia (n = 61) and four ancient maritime individuals from Patagonia (∼1,000 y old). Both the modern and ancient individuals studied in this work have a greater genetic affinity with other modern Native Americans than to any non-American population, showing within South America a clear structure between major geographical regions. Native Patagonian Kawéskar and Yámana showed the highest genetic affinity with the ancient individuals, indicating genetic continuity in the region during the past 1,000 y before present, together with an important agreement between the ethnic affiliation and historical distribution of both groups. Lastly, the ancient maritime individuals were genetically equidistant to a ∼200-y-old terrestrial hunter-gatherer from Tierra del Fuego, which supports a model with an initial separation of a common ancestral group to both maritime populations from a terrestrial population, with a later diversification of the maritime groups.

pca-ancient-south-american
PCA of ancient and present-day South American populations. All of the ancient individuals were projected onto the first two PCs by using the lsq option from smartpca.

Related:

Earliest modern humans outside Africa and ancient genomic history

palaeolithic

Interesting new paper at Science, The earliest modern humans outside Africa, by Hershkovitz et al., Science (2018) Vol. 359, Issue 6374, pp. 456-459

Introduction:

Recent paleoanthropological studies have suggested that modern humans migrated from Africa as early as the beginning of the Late Pleistocene, 120,000 years ago. Hershkovitz et al. now suggest that early modern humans were already present outside of Africa more than 55,000 years earlier (see the Perspective by Stringer and Galway-Witham). During excavations of sediments at Mount Carmel, Israel, they found a fossil of a mouth part, a left hemimaxilla, with almost complete dentition.

The sediments contain a series of well-defined hearths and a rich stone-based industry, as well as abundant animal remains. Analysis of the human remains, and dating of the site and the fossil itself, indicate a likely age of at least 177,000 years for the fossil—making it the oldest member of the Homo sapiens clade found outside Africa.

Abstract

To date, the earliest modern human fossils found outside of Africa are dated to around 90,000 to 120,000 years ago at the Levantine sites of Skhul and Qafzeh. A maxilla and associated dentition recently discovered at Misliya Cave, Israel, was dated to 177,000 to 194,000 years ago, suggesting that members of the Homo sapiens clade left Africa earlier than previously thought. This finding changes our view on modern human dispersal and is consistent with recent genetic studies, which have posited the possibility of an earlier dispersal of Homo sapiens around 220,000 years ago. The Misliya maxilla is associated with full-fledged Levallois technology in the Levant, suggesting that the emergence of this technology is linked to the appearance of Homo sapiens in the region, as has been documented in Africa.

Beautifully complementing this anthropological research, the open access review Insights into Modern Human Prehistory Using Ancient Genomes, by Melinda A. Yang and Qiaomei Fu, Trends in Genetics (2018), depicts potential later migrations:

eurasia-americas-populations
Key Figure: Schematic of Populations in Eurasia and the Americas (Bottom Right) during Ancient Modern A (AMA, ∼45–35 ka), Ancient Modern B (AMB, ∼34–15 ka), and Ancient Modern C (AMC, ∼14–7.5 ka).

Abbreviations: AMER, ancestry related to present-day Native Americans and Anzick 1; ANE, ancestry related to ancient North Eurasians represented by Mal’ta 1; EAS, ancestry related to present-day East Asians and the Tianyuan and Devil’s Gate individuals; EUR, ancestry related to ancient Europeans and found partially in present-day Europeans; NE, ancestry related to an unsampled population known as Basal Eurasian and found in partial amounts in ancient and present-day populations of the Near East and in present-day Europeans. Broken lines indicate no ancient genetic samples have been found for a population with the inferred ancestry. Colors loosely indicate genetic groupings between or within a region, with color gradients showing the connections (i.e., gene flow) that may exist between different ancient populations. A summary of major events in each of the time periods is on the left.

Summary:

Eurasia ∼45–35 ka shows the presence of at least four distinct populations: early Asians and Europeans, as well as populations with ancestry found hardly or not at all in present-day populations.

Europeans from around 34–15 ka show high internal population structure.

Approximately 14–7.5 ka, populations across Eurasia shared genetic similarities, suggesting greater interactions between geographically distant populations.

Ancient modern human genomes support at least two Neanderthal admixture events, one ∼60–50 ka in early ancestors of non-African populations and a second >37 ka related to the Oase 1 individual.

A gradual decline in archaic ancestry in Europeans dating from ∼37 to 14 ka suggests that purifying selection lowered the amount of Neanderthal ancestry first introduced into ancient modern humans.

The genetic relationship of past modern humans to today’s populations and each other was largely unknown until recently, when advances in ancient DNA sequencing allowed for unprecedented analysis of the genomes of these early people. These ancient genomes reveal new insights into human prehistory not always observed studying present-day populations, including greater details on the genetic diversity, population structure, and gene flow that characterized past human populations, particularly in early Eurasia, as well as increased insight on the relationship between archaic and modern humans. Here, we review genetic studies on ∼45 000- to 7500-year-old individuals associated with mainly preagricultural cultures found in Eurasia, the Americas, and Africa.

(Both articles discovered via Iosif Lazaridis Twitter account).

See also:

Ancient mtDNA from Central America and Mexico

pre-columbian-central-america-mexico

New article, Successful reconstruction of whole mitochondrial genomes from ancient Central America and Mexico, by Morales-Arce et al., Scientific Reports (2017).

Abstract:

The northern and southern peripheries of ancient Mesoamerica are poorly understood. There has been speculation over whether borderland cultures such as Greater Nicoya and Casas Grandes represent Mesoamerican outposts in the Isthmo-Colombian area and the Greater Southwest, respectively. Poor ancient DNA preservation in these regions challenged previous attempts to resolve these questions using conventional genetic techniques. We apply advanced in-solution mitogenome capture and high-throughput sequencing to fourteen dental samples obtained from the Greater Nicoya sites of Jícaro and La Cascabel in northwest Costa Rica (n = 9; A.D. 800–1250) and the Casas Grandes sites of Paquimé and Convento in northwest Mexico (n = 5; A.D. 1200–1450). Full mitogenome reconstruction was successful for three individuals from Jícaro and five individuals from Paquimé and Convento. The three Jícaro individuals belong to haplogroup B2d, a haplogroup found today only among Central American Chibchan-speakers. The five Paquimé and Convento individuals belong to haplogroups C1c1a, C1c5, B2f and B2a which, are found in contemporary populations in North America and Mesoamerica. We report the first successfully reconstructed ancient mitogenomes from Central America, and the first genetic evidence of ancestry affinity of the ancient inhabitants of Greater Nicoya and Casas Grandes with contemporary Isthmo-Columbian and Greater Southwest populations, respectively.

mesoamerica-ancient-mtdna
Archaeological sites location and corresponding culture areas as noted in the text. ArcGIS 10.4 software (http://www.esri.com/software/arcgis) was used to generate the figure. Service layer credits Esri, ArcGIS Online, TerraColor (Earthstar Geographics) 1999; Vivid – Mexico (Digital Globe) 2005, 2009, 2010, 2011, 2012, 2013, 2014, 2015; Metro (Digital Globe) 2016; Vivid Caribbean (Digital Globe) 2013, 2014, 2015, 2016, Vivid (Digital Globe) 2015, Vivid – Mexico (Digital Globe) 2012 and the GIS User Community.

Discovered via Bernard Sécher’s blog.

Featured image: From Wikipedia, author Juan Miguel, “Mesoamérica y toda América Central prehispanica en el siglo XVI (16) — antes de la llegada de los españoles.”

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