Ancient mitogenomes from the Southern Pampas of Argentina reflect local differentiation and limited extra-regional linkages after rapid initial colonization.

OBJECTIVE: This study aims to contribute to the recovery of Indigenous evolutionary history in the Southern Pampas region of Argentina through an analysis of ancient complete mitochondrial genomes. MATERIALS AND METHODS: We generated DNA data for nine complete mitogenomes from the Southern Pampas, dated to between 2531 and 723 cal BP. In combination with previously published ancient mitogenomes from the region and from throughout South America, we documented instances of extra-regional lineage-sharing, and estimated coalescent ages for local lineages using a Bayesian method with tip calibrations in a phylogenetic analysis. RESULTS: We identified a novel mitochondrial haplogroup, B2b16, and two recently defined haplogroups, A2ay and B2ak1, as well as three local haplotypes within founder haplogroups C1b and C1d. We detected lineage-sharing with ancient and contemporary individuals from Central Argentina, but not with ancient or contemporary samples from North Patagonian or Littoral regions of Argentina, despite archeological evidence of cultural interactions with the latter regions. The estimated coalescent age of these shared lineages is ~10,000 years BP. DISCUSSION: The history of the human populations in the Southern Pampas is temporally deep, exhibiting long-term continuity of mitogenome lineages. Additionally, the identification of highly localized mtDNA clades accords with a model of relatively rapid initial colonization of South America by Indigenous communities, followed by more local patterns of limited gene flow and genetic drift in various South American regions, including the Pampas.

Ancient DNA analysis reveals temporal and geographical patterns of mitochondrial diversity in pre-Hispanic populations from Central Argentina.

OBJECTIVES: The study of the ancient populations of Central Argentina has a crucial importance for our understanding of the evolutionary processes in the Southern Cone of South America, given its geographic position as a crossroads. Therefore, the aim of this study is to evaluate the temporal and geographical patterns of genetic variation among the groups that inhabited the current territory of Córdoba Province during the Middle and Late Holocene. METHODS: We analyzed the mitochondrial haplogroups of 74 individuals and 46 Hypervariable Region I (HVR-I) sequences, both novel and previously reported, from archeological populations of the eastern Plains and western Sierras regions of the province of Córdoba. The HVR-I sequences were also compared with other ancient groups from Argentina and with present-day populations from Central Argentina by pairwise distance analysis and identification of shared haplotypes. RESULTS: Significant differences in haplogroup and haplotype distributions between the two geographical regions were found. Sierras showed genetic affinities with certain ancient populations of Northwestern Argentina, while Plains resembled its neighbors from Santiago del Estero Province and the Pampas region. We did not observe genetic differences among the pre 1200 and post 1200 yBP temporal subsets of individuals defined by the emergence of horticulture, considering both geographical samples jointly. CONCLUSIONS: The observed patterns of geographical heterogeneity could indicate the existence of biologically distinct populations inhabiting the mountainous region and the eastern plains of Córdoba Province in pre-Hispanic times. Maternal lineages analyses support a scenario of local evolution with great temporal depth in Central Argentina, with continuity until the present.

Ancient and modern mitogenomes from Central Argentina: new insights into population continuity, temporal depth and migration in South America.

The inverted triangle shape of South America places Argentina territory as a geographical crossroads between the two principal peopling streams that followed either the Pacific or the Atlantic coasts, which could have then merged in Central Argentina (CA). Although the genetic diversity from this region is therefore crucial to decipher past population movements in South America, its characterization has been overlooked so far. We report 92 modern and 22 ancient mitogenomes spanning a temporal range of 5000 years, which were compared with a large set of previously reported data. Leveraging this dataset representative of the mitochondrial diversity of the subcontinent, we investigate the maternal history of CA populations within a wider geographical context. We describe a large number of novel clades within the mitochondrial DNA tree, thus providing new phylogenetic interpretations for South America. We also identify several local clades of great temporal depth with continuity until the present time, which stem directly from the founder haplotypes, suggesting that they originated in the region and expanded from there. Moreover, the presence of lineages characteristic of other South American regions reveals the existence of gene flow to CA. Finally, we report some lineages with discontinuous distribution across the Americas, which suggest the persistence of relic lineages likely linked to the first population arrivals. The present study represents to date the most exhaustive attempt to elaborate a Native American genetic map from modern and ancient complete mitochondrial genomes in Argentina and provides relevant information about the general process of settlement in South America.

Biological kinship in 750 year old human remains from Central Argentina with signs of interpersonal violence.

Human skeletal remains of an adult male (20-24 years old) and a juvenile (4-8 years old), dated to 750 ± 85 14C years BP, were found on the southern margin of Mar Chiquita Lagoon (Córdoba, Argentina). Both individuals show signs of being victims of interpersonal violence, with arrowheads associated with the remains and perimortem lesions on the juvenile, as well as an unusual form of burial, with the juvenile partially overlapped with the adult. The aim of this work is to study a possible kin relationship between these two individuals through ancient DNA analysis. Biological kinship was evaluated by autosomal and Y-chromosome STR (short tandem repeat) typing, PCR-APLP for SNP determination and hypervariable region I sequencing of the mitochondrial DNA. Genetic analyses indicated that these individuals shared the same Y-chromosomal haplotype but different mitochondrial lineages. The likelihood ratio based on autosomal loci indicates that the genetic profiles of the human remains would be more likely to be that indicating a father-son bond. The paleogenetic approach combined with forensic genetic methods applied to this study allowed us to confirm a hypothesis that originated in bioarchaeological evidence. This study constitutes a unique case in Argentina of kinship determination based on DNA profiles of human remains in an archaeological context of interpersonal violence. It is important to highlight the contribution made by these studies to address topics usually hidden in bioarchaeological studies, such as community organization, cultural customs and mortuary practices.

Fine-scale genomic analyses of admixed individuals reveal unrecognized genetic ancestry components in Argentina.

Similarly to other populations across the Americas, Argentinean populations trace back their genetic ancestry into African, European and Native American ancestors, reflecting a complex demographic history with multiple migration and admixture events in pre- and post-colonial times. However, little is known about the sub-continental origins of these three main ancestries. We present new high-throughput genotyping data for 87 admixed individuals across Argentina. This data was combined to previously published data for admixed individuals in the region and then compared to different reference panels specifically built to perform population structure analyses at a sub-continental level. Concerning the Native American ancestry, we could identify four Native American components segregating in modern Argentinean populations. Three of them are also found in modern South American populations and are specifically represented in Central Andes, Central Chile/Patagonia, and Subtropical and Tropical Forests geographic areas. The fourth component might be specific to the Central Western region of Argentina, and it is not well represented in any genomic data from the literature. As for the European and African ancestries, we confirmed previous results about origins from Southern Europe, Western and Central Western Africa, and we provide evidences for the presence of Northern European and Eastern African ancestries.

Genetic variation in populations from central Argentina based on mitochondrial and Y chromosome DNA evidence.

We present new data and analysis on the genetic variation of contemporary inhabitants of central Argentina, including a total of 812 unrelated individuals from 20 populations. Our goal was to bring new elements for understanding micro-evolutionary and historical processes that generated the genetic diversity of the region, using molecular markers of uniparental inheritance (mitochondrial DNA and Y chromosome). Almost 76% of the individuals show mitochondrial lineages of American origin. The Native American haplogroups predominate in all surveyed localities, except in one. The larger presence of Eurasian maternal lineages were observed in the plains (Pampas) of the southeast, whereas the African lineages are more frequent in northern Córdoba. On the other hand, the analysis of 258 male samples reveals that 92% of them present Eurasian paternal lineages, 7% carry Native American haplogroups, and only 1% of the males show African lineages. The maternal lineages have high genetic diversity homogeneously distributed throughout central Argentina, probably as result of a recent common origin and sustained gene flow. Migratory events that occurred in colonial and recent times should have contributed to hiding any traces of differentiation that might have existed in the past. The analysis of paternal lineages showed also homogeneous distribution of the variation together with a drastic reduction of the native male population.

A tale of agriculturalists and hunter-gatherers: Exploring the thrifty genotype hypothesis in native South Americans.

OBJECTIVES: To determine genetic differences between agriculturalist and hunter-gatherer southern Native American populations for selected metabolism-related markers and to test whether Neel's thrifty genotype hypothesis (TGH) could explain the genetic patterns observed in these populations. MATERIALS AND METHODS: 375 Native South American individuals from 17 populations were genotyped using six markers (APOE rs429358 and rs7412; APOA2 rs5082; CD36 rs3211883; TCF7L2 rs11196205; and IGF2BP2 rs11705701). Additionally, APOE genotypes from 39 individuals were obtained from the literature. AMOVA, main effects, and gene-gene interaction tests were performed. RESULTS: We observed differences in allele distribution patterns between agriculturalists and hunter-gatherers for some markers. For instance, between-groups component of genetic variance (FCT ) for APOE rs429358 showed strong differences in allelic distributions between hunter-gatherers and agriculturalists (p = 0.00196). Gene-gene interaction analysis indicated that the APOE E4/CD36 TT and APOE E4/IGF2BP2 A carrier combinations occur at a higher frequency in hunter-gatherers, but this combination is not replicated in archaic (Neanderthal and Denisovan) and ancient (Anzick, Saqqaq, Ust-Ishim, Mal'ta) hunter-gatherer individuals. DISCUSSION: A complex scenario explains the observed frequencies of the tested markers in hunter-gatherers. Different factors, such as pleotropic alleles, rainforest selective pressures, and population dynamics, may be collectively shaping the observed genetic patterns. We conclude that although TGH seems a plausible hypothesis to explain part of the data, other factors may be important in our tested populations.

Molecular polymorphisms of the ABO locus as informative markers of ancestry in Central Argentina.

OBJECTIVES: The aim of this study was to investigate the distribution of molecular polymorphisms of the ABO gene in four population samples from the province of Córdoba, in Central Argentina, and to compare them with other worldwide populations. METHODS: A total of 110 buccal swab samples from autochthonous individuals of Córdoba were typified. Molecular characterization of the allelic variants was performed by the analysis of exons 6 and 7 of the ABO gene using PCR-RFLP analysis. Additionally, the Native American AIM O1v542 was characterized by direct sequencing. RESULTS: The four Córdoba populations did not show significant geographic structure, although the frequency of the O1v542 haplotype, detected in all the populations studied, ranged from 0.019 to 0.222. The principal component analysis based on O allele distribution showed that the populations from Córdoba clustered close to the admixed populations of Santiago and Mexico City, and at intermediate distances between European and Native American populations, while being distant from the African population. CONCLUSIONS: The results demonstrate that the analysis of the ABO system constitutes a useful tool for the study of the genetic structure and evolutionary history of human populations, reflecting accurately the relative contribution of parental continental contribution to the gene pool of admixed populations.

So close, so far away: analysis of surnames in a town of twins (Cândido Godói, Brazil).

Cândido Godói is a small Brazilian town known for high rates of twin birth. In 2011, a genetic study showed that this localized high rate of twin births could be explained by a genetic founder effect. Here we used isonymic analysis and surname distribution to identify population subgroups within 5316 inhabitants and 665 different surnames. Four clusters were constructed based on different twin rates (P < 0.001; MRPP test). Fisher's α and consanguinity index showed low and high values, respectively, corresponding with observed values in isolated communities with high levels of genetic drift. Values of A and B estimators confirmed population isolation. Three boundaries were identified with Monmonier's maximum difference algorithm (P = 0.007). Inside the isolated sections, surnames of different geographic origins, language, and religion were represented. With an adequate statistical methodology, surname analyses provided a close approximation of historic and socioeconomic background at the moment of colony settlement. In this context, the maintenance of social and cultural practices had strong implications for the population's structure leading to drift processes in this small town, supporting the previous genetic study.

Analysis of uniparental lineages in two villages of Santiago Del Estero, Argentina, seat of Pueblos de Indios in colonial times.

Based on the analysis of the mitochondrial control region and seven biallelic markers of the Y chromosome, we investigated the genetic composition of two rural populations of southern Santiago del Estero, Argentina, that were seats in colonial times of pueblos de indios, a colonial practice that consisted of concentrating the indigenous populations in organized and accessible settlements, to facilitate Christianizing and policing. We found the Native American Y chromosome haplogroup Q1a3a in only 11% (3 of 27) of the males. Haplogroup R, common in European populations, is the most frequent haplogroup in Santiago del Estero (55%). In contrast, the persistence of Native American maternal lineages is extremely high (95%). This finding is most likely due to the low incidence in that region of the 20th century European wave of migration and to the existence of pueblos de indios from 1612 to the first decades of the 19th century. In contrast to archeological records that suggest Santiago del Estero late pre-Hispanic groups were strongly influenced by the Andean world, we did not find genetic evidence in support of significant gene fl ow. On the other hand, these populations share many mitochondrial DNA hypervariable region I (HVRI) haplotypes with other populations from the Sierras Pampeanas (particularly with Córdoba) and the Gran Chaco regions.

Phylogeography of mitochondrial haplogroup D1: an early spread of subhaplogroup D1j from Central Argentina.

We analyzed the patterns of variation of haplogroup D1 in central Argentina, including new data and published information from other populations of South America. Almost 28% (107/388) of the individuals sampled in the region belong to haplogroup D1, whereas more than 52% of them correspond to the recently described subhaplogroup D1j (Bodner et al.: Genome Res 22 (2012) 811-820), defined by the presence of additional transitions at np T152C-C16242T-T16311C to the nodal D1 motif. This lineage was found at high frequencies across a wide territory with marked geographical-ecological differences. Additionally, 12 individuals present the mutation C16187T that defines the recently named subhaplogroup D1g (Bodner et al.: Genome Res 22 (2012) 811-820), previously described in populations of Patagonia and Tierra del Fuego. Based on our results and additional data already published, we postulate that the most likely origin of subhaplogroup D1j is the region of Sierras Pampeanas, which occupies the center and part of the northwestern portion of Argentina. The extensive yet restricted geographical distribution, the relatively large internal diversity, and the absence or low incidence of D1j in other regions of South America suggest the existence of an ancient metapopulation covering the Sierras Pampeanas, being this lineage its genetic signature. Further support for a scenario of local origin for D1j in the Sierras Pampeanas stems from the fact that early derivatives from a putative ancestral lineage carrying the transitions T16311C-T152C have only been found in this region, supporting the hypothesis that it might represent an ancestral motif previous to the appearance of D1j-specific change C16242T.

Geographic patterns of craniofacial variation in pre-Hispanic populations from the Southern Cone of South America.

In this study we analyzed the relationships and patterns of spatial variation from morphological cranial variability of 17 population samples representing the ancient inhabitants of the central territory of Argentina (archaeologically known as "Sierras Centrales") and other pre-Hispanic populations from different ecological and geographic regions of the Southern Cone of South America (Argentina and Uruguay), based on the analysis of 10 craniofacial measurements. Results obtained from D2 distances can be interpreted as evidence of a similar biological history for the populations that inhabited the Sierras Centrales and the population of Santiago del Estero. Matrix correlation analysis demonstrated that craniometric variation is significantly influenced by geography, suggesting that populations that lived at lower geographical distance share more biological similarity. Global spatial autocorrelation analysis suggests a clinal pattern for the biological variation, although Moran's I estimates calculated for each variable demonstrate that only nasal height and breadth show this spatial pattern of variation. Results from spatial regression techniques show a significant effect of altitude modeling nasal shape, in agreement with previous studies suggesting that nasal morphology is strongly influenced by environment variables.

Incidence and distribution of Native American mtDNA haplogroups in central Argentina.

We report the incidence and distribution of Native American mtDNA haplogroups in nine villages across the Sierras Centrales archeological area, located in central Argentina. The aims of the study were (1) to investigate the relative incidence of native maternal lineages, (2) to determine whether or not the homogeneous pattern observed in a previous study persists at this larger scale, and (3) to ascertain the genetic affinities between the studied population and other native populations of the Southern Cone of South America. Of the 310 individuals from whom DNA was extracted, 249 (80.3%) were assigned to one of the founding native American haplogroups. This finding confirms the persistence at high prevalence of native maternal lineages in the rural populations of central Argentina. The haplogroup distribution is homogeneous in the population samples from Córdoba province, with haplogroups C and D always found at the highest frequencies. The sample from San Luis province, Tilisarao, presents a different genetic pattern, with haplogroups A and B being the most frequent. Principal components analysis and SAMOVA at the regional level show that the Córdoba, Patagonia, and Tierra del Fuego populations cluster together, which suggests a common origin.

Brief communication: Restricted geographic distribution for Y-Q* paragroup in South America.

We analyzed 21 paragroup Q* Y chromosomes from South American aboriginal and urban populations. Our aims were to evaluate the phylogenetic status, geographic distribution, and genetic diversity in these groups of chromosomes and compare the degree of genetic variation in relation to Q1a3a haplotypes. All Q* chromosomes from our series and five samples from North American Q* presented the derivate state for M346, that is present upstream to M3, and determined Q1a3* paragroup. We found a restrictive geographic distribution and low frequency of Q1a3* in South America. We assumed that this low frequency could be reflecting extreme drift effects. However, several estimates of gene diversity do not support the existence of a severe bottleneck. The mean haplotype diversity expected was similar to that for South American Q1a3* and Q1a3a (0.478 and 0.501, respectively). The analysis of previous reports from other research groups and this study shows the highest frequencies of Q* for the West Corner and the Grand Chaco regions of South America. At present, there is no information on whether the phylogenetic status of Q* paragoup described in previous reports is similar to that of Q1a3* paragroup though our results support this possibility.

Linkage disequilibrium patterns and genetic structure of Amerindian and non-Amerindian Brazilian populations revealed by long-range X-STR markers.

The extent of X-chromosome linkage disequilibrium (LD) was studied in a southern Brazilian population, and in a pool of samples from Amerindian populations. For this purpose, 11 microsatellites, located mostly in a Xq region comprising approximately 86 Mb was investigated. The lower Amerindian gene diversity associated with significant differences between the populations studied indicated population structure as the main cause for the higher LD values in the Amerindian pool. On the other hand, the LD levels of the non-Amerindian Brazilian sample, although less extensive than that of the Amerindians, were probably determined by admixture events. Our results indicated that different demographic histories have significant effects on LD levels of human populations, and provide a first approach to the X-chromosome ancestry of Amerindian and non-Amerindian Brazilian populations, being valuable for future studies involving mapping and population genetic studies.

Autosomal STR genetic variability in the Gran Chaco native population: Homogeneity or heterogeneity?

To investigate the population structure and variation in Gran Chaco's Amerindian population, data from 15 short tandem repeats (STRs) were determined in 128 individuals from three tribes of the Argentinean part of this region. STR genotypic differences, structure analysis, and multidimensional plot for the D(A) distances indicated that (1) Wichí from the Chaco Province are genetically distinct from the other populations, but still preserve a fair amount of genetic similarity with Wichí from Formosa; (2) the Toba populations studied are genetically indistinguishable; and (3) Toba subjects from Formosa are similar to the Pilagá of the same linguistic group (Guaykurú) and to the Wichí from Formosa who speak a Mataco language. This similarity could be due to their past mobility and the custom of absorbing females taken as prisoners from groups raided by them. Language, geography, and genetics seem to play similar roles in determining the population structure of these groups. Analyses of molecular variance and G(ST)' values calculated considering three South American regions indicated that the Argentinean Chaco is genetically homogeneous; addition of the Ayoreo Amerindians of the Paraguayan Chaco, however, led to diversity values that are not much different from those of South Amerindians in general. The present data contribute to efforts that try to understand in what way groups with diverse sociocultural settings (tribal, agricultural, and industrial) differ in genetic structure.

Human colonization of the central territory of Argentina: design matrix models and craniometric evidence.

In this study we test several hypotheses about the peopling of the central territory of Argentina, archaeologically known as Sierras Centrales, by testing the association between four alternative models of the peopling of the area and cranial morphological variation through distance and matrix correlation analyses. Our results show that the ancient inhabitants of Sierras Centrales demonstrated close morphological similarities with the Patagonian and Tierra del Fuego populations. Moreover, the correlation and partial correlation analyses suggest that the peopling of the Sierras Centrales most likely took place as a migratory wave proceeding from the present area of Northeastern Argentina, and continued southward to Patagonia and Tierra del Fuego.

Is the genetic structure of Gran Chaco populations unique? Interregional perspectives on native South American mitochondrial DNA variation.

This study reevaluates the hypothesis in Demarchi et al. (2001 Am. J. Phys. Anthropol. 115:199-203) that Gran Chaco peoples demonstrate a unique pattern of genetic diversity due to a distinct regional population history. Specifically, they found populations in the central part of the Gran Chaco, or Central Chaco, to have higher within- and lower between-population mitochondrial DNA (mtDNA) haplogroup frequency variation compared to populations in other South American regions. To test this hypothesis of regional uniqueness, we applied analytical and simulation methods to mtDNA first hypervariable (HVI) region sequence data from a broad set of comparative South and Central American population samples. Contrary to the results of Demarchi et al. (2001 Am. J. Phys. Anthropol. 115:199-203), we found that the Gran Chaco's regional within-population diversity is about average among regions, and populations are highly differentiated from each other. When we limited the scale of analysis to the Central Chaco, a more localized subregion of the Gran Chaco, our results fell more in line with the original findings of Demarchi et al. (2001 Am. J. Phys. Anthropol. 115:199-203). Still, we conclude that neither the Gran Chaco regional pattern, nor the Central Chaco subregional pattern, is unique within South America. Nonetheless, the Central Chaco pattern accords well with the area's history, including pre-European contact lifeways and the documented historical use of the area as an interregional crossroads. However, we cannot exclude post-European contact disruption of traditional mating networks as an equally plausible explanation for the observed diversity pattern. Finally, these results additionally inform broader models of South American genetic diversity. While other researchers proposed an east-west continental division in patterns of genetic variation (e.g., Fuselli et al. 2003 Mol. Biol. Evol. 20:1682-1691), we found that in the geographically intermediate Central Chaco, a strict east-west divide in genetic variation breaks down. We suggest that future genetic characterizations of the continent, and subsequent interpretations of evolutionary history, involve a broad regional sampling of South American populations.

Y-chromosomal evidence for a founder effect in Mbyá-guaraní Amerindians from northeast Argentina.

To assess the paternal history of the Mbyá-Guaraní Amerindians of northeast Argentina, we examined the genetic variation in seven Y-chromosome loci: the binary marker M3 at locus DYS199, and six short tandem repeats (DYS19, DYS389I, DYS389II, DYS390, DYS391, and DYS393). The most striking finding is the high frequency among the Mbyá-Guaraní of Q3 lineages with the usually rare alleles DYS391*11 and DYS393*11, which could be the result of a founder effect, given the recent history of the population.

Distribution of a 9.1-kb insertion-deletion polymorphism among native and admixed populations from Argentina.

We studied five population samples from Argentina, four drawn from Native American groups of the northeast region (Wichí, Pilagá, Toba, and Mbyá-Guaraní) and one from two small villages of the Córdoba province. In this study we report genotypes and allele frequencies of the 9.1-kb insertion-deletion polymorphism located on chromosome 22. The frequency of the deletion allele ranges from 0.276 in the Mbyá-Guaraní to 0.470 in the Pilagá. The coefficient of population differentiation is fairly low (F(ST) = 0.013), does not reflect any geographic or linguistic pattern, and seems to be more related to stochastic processes than to directional forces.