Genetic variation and population structure in native Americans

We examined genetic diversity and population structure in the American landmass using 678 autosomal microsatellite markers genotyped in 422 individuals representing 24 Native American populations sampled from North, Central, and South America. These data were analyzed jointly with similar data available in 54 other indigenous populations worldwide, including an additional five Native American groups. The Native American populations have lower genetic diversity and greater differentiation than populations from other continental regions. We observe gradients both of decreasing genetic diversity as a function of geographic distance from the Bering Strait and of decreasing genetic similarity to Siberians--signals of the southward dispersal of human populations from the northwestern tip of the Americas. We also observe evidence of: (1) a higher level of diversity and lower level of population structure in western South America compared to eastern South America, (2) a relative lack of differentiation between Mesoamerican and Andean populations, (3) a scenario in which coastal routes were easier for migrating peoples to traverse in comparison with inland routes, and (4) a partial agreement on a local scale between genetic similarity and the linguistic classification of populations. These findings offer new insights into the process of population dispersal and differentiation during the peopling of the Americas.     

Predictions of native American population structure using linguistic covariates in a hidden regression framework

Background

The mainland of the Americas is home to a remarkable diversity of languages, and the relationships between genes and languages have attracted considerable attention in the past. Here we investigate to which extent geography and languages can predict the genetic structure of Native American populations.

Methodology/Principal Findings

Our approach is based on a Bayesian latent cluster regression model in which cluster membership is explained by geographic and linguistic covariates. After correcting for geographic effects, we find that the inclusion of linguistic information improves the prediction of individual membership to genetic clusters. We further compare the predictive power of Greenberg''s and The Ethnologue classifications of Amerindian languages. We report that The Ethnologue classification provides a better genetic proxy than Greenberg''s classification at the stock and at the group levels. Although high predictive values can be achieved from The Ethnologue classification, we nevertheless emphasize that Choco, Chibchan and Tupi linguistic families do not exhibit a univocal correspondence with genetic clusters.

Conclusions/Significance

The Bayesian latent class regression model described here is efficient at predicting population genetic structure using geographic and linguistic information in Native American populations.     

The impact of group fissions on genetic structure in Native South America and implications for human evolution

In a series of publications beginning in the 1960s, Neel and colleagues suggested that genetically nonrandom, or "lineal", population fissions contributed to genetic structure in ancient human groups. The authors reached this conclusion by studying the genetic consequences of village fissions among the Yanomamo, a Native South American group thought to have been relatively unaffected by European contact and, therefore, representative of the human past. On the basis of ethnographic accounts and pedigree data, they further concluded that patrilineal relationships were particularly important in shaping the genetic structure of villages following fissions. This study reexamines the genetic consequences of village fissions using autosomal STRs, Y-chromosome STRs, and mitochondrial DNA sequences collected from large samples of individuals from multiple Yanomamo villages. Our analyses of the autosomal STRs replicate the previous finding that village fissions have produced substantial genetic structure among the Yanomamo. However, our analyses of Y-chromosome STRs and mtDNA d-loop polymorphisms suggest that other population processes, including village movements, inter-village migration, and polygynous marriage, affect genetic structure in ways not predicted by a simple model of patrilineal fissions. We discuss the broader implications of population fissions for human evolution and the suitability of using the Yanomamo as a model for the human past.     

Genetic divergence disclosing a rapid prehistorical dispersion of native americans in central and South america

An accurate estimate of the divergence time between Native Americans is important for understanding the initial entry and early dispersion of human beings in the New World. Current methods for estimating the genetic divergence time of populations could seriously depart from a linear relationship with the true divergence for multiple populations of a different population size and significant population expansion. Here, to address this problem, we propose a novel measure to estimate the genetic divergence time of populations. Computer simulation revealed that the new measure maintained an excellent linear correlation with the population divergence time in complicated multi-population scenarios with population expansion. Utilizing the new measure and microsatellite data of 21 Native American populations, we investigated the genetic divergences of the Native American populations. The results indicated that genetic divergences between North American populations are greater than that between Central and South American populations. None of the divergences, however, were large enough to constitute convincing evidence supporting the two-wave or multi-wave migration model for the initial entry of human beings into America. The genetic affinity of the Native American populations was further explored using Neighbor-Net and the genetic divergences suggested that these populations could be categorized into four genetic groups living in four different ecologic zones. The divergence of the population groups suggests that the early dispersion of human beings in America was a multi-step procedure. Further, the divergences suggest the rapid dispersion of Native Americans in Central and South Americas after a long standstill period in North America.     

Linguistic and maternal genetic diversity are not correlated in Native Mexicans

Mesoamerica, defined as the broad linguistic and cultural area from middle southern Mexico to Costa Rica, might have played a pivotal role during the colonization of the American continent. The Mesoamerican isthmus has constituted an important geographic barrier that has severely restricted gene flow between North and South America in pre-historical times. Although the Native American component has been already described in admixed Mexican populations, few studies have been carried out in native Mexican populations. In this study, we present mitochondrial DNA (mtDNA) sequence data for the first hypervariable region (HVR-I) in 477 unrelated individuals belonging to 11 different native populations from Mexico. Almost all of the Native Mexican mtDNAs could be classified into the four pan-Amerindian haplogroups (A2, B2, C1, and D1); only two of them could be allocated to the rare Native American lineage D4h3. Their haplogroup phylogenies are clearly star-like, as expected from relatively young populations that have experienced diverse episodes of genetic drift (e.g., extensive isolation, genetic drift, and founder effects) and posterior population expansions. In agreement with this observation, Native Mexican populations show a high degree of heterogeneity in their patterns of haplogroup frequencies. Haplogroup X2a was absent in our samples, supporting previous observations where this clade was only detected in the American northernmost areas. The search for identical sequences in the American continent shows that, although Native Mexican populations seem to show a closer relationship to North American populations, they cannot be related to a single geographical region within the continent. Finally, we did not find significant population structure in the maternal lineages when considering the four main and distinct linguistic groups represented in our Mexican samples (Oto-Manguean, Uto-Aztecan, Tarascan, and Mayan), suggesting that genetic divergence predates linguistic diversification in Mexico.     

The Uto‐Aztecan premolar among North and South Amerindians: Geographic variation and genetics

The Uto‐Aztecan premolar (UAP) is a dental polymorphism characterized by an exaggerated distobuccal rotation of the paracone in combination with the presence of a fossa at the intersection of the distal occlusal ridge and distal marginal ridge of upper first premolars. This trait is important because, unlike other dental variants, it has been found exclusively in Native American populations. However, the trait's temporal and geographic variation has never been fully documented. The discovery of a Uto‐Aztecan premolar in a prehistoric skeletal series from northern South America calls into question the presumed linguistic and geographic limits of this trait. We examined published and unpublished data for this rare but highly distinctive trait in samples representing over 5,000 Native Americans from North and South America. Our findings in living Southwest Amerindian populations corroborate the notion that the variable goes beyond the bounds of the Uto‐Aztecan language family. It is found in prehistoric Native Americans from South America, eastern North America, Northern and Central Mexico, and in living and prehistoric populations in the American Southwest that are not members of the Uto‐Aztecan language stock. The chronology of samples, its geographic distribution, and trait frequencies suggests a North American origin (Southwest) for UAP perhaps between 15,000 BP and 4,000 BP and a rapid and widespread dispersal into South America during the late Holocene. Family data indicate that it may represent an autosomal recessive mutation that occurred after the peopling of the Americas as its geographic range appears to be limited to North and South Amerindian populations. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Genetic differences between Chibcha and Non-Chibcha speaking tribes based on mitochondrial DNA (mtDNA) haplogroups from 21 Amerindian tribes from Colombia

We analyzed the frequency of four mitochondrial DNA haplogroups in 424 individuals from 21 Colombian Amerindian tribes. Our results showed a high degree of mtDNA diversity and genetic heterogeneity. Frequencies of mtDNA haplogroups A and C were high in the majority of populations studied. The distribution of these four mtDNA haplogroups from Amerindian populations was different in the northern region of the country compared to those in the south. Haplogroup A was more frequently found among Amerindian tribes in northern Colombia, while haplogroup D was more frequent among tribes in the south. Haplogroups A, C and D have clinal tendencies in Colombia and South America in general. Populations belonging to the Chibcha linguistic family of Colombia and other countries nearby showed a strong genetic differentiation from the other populations tested, thus corroborating previous findings. Genetically, the Ingano, Paez and Guambiano populations are more closely related to other groups of south eastern Colombia, as also inferred from other genetic markers and from archeological data. Strong evidence for a correspondence between geographical and linguistic classification was found, and this is consistent with evidence that gene flow and the exchange of customs and knowledge and language elements between groups is facilitated by close proximity.     

Phylogenetic information in polymorphic L1 and Alu insertions from East Asians and Native American populations

This study attempts to ascertain genetic affinities between Native American and East Asian populations by analyzing four polymorphic Alu insertions (PAIs) and three L1 polymorphic loci. These two genetic systems demonstrated strong congruence when levels of diversity and genetic distances were considered. Overall, genetic relatedness within Native American groups does not correlate with geographical and linguistic structure, although strong grouping for Native Americans with East Asians was demonstrated, with clear discrimination from African and European groups. Most of the variation was assigned to differences occurring within groups, but the interpopulation variation found for South Amerindians was recognizably higher in comparison to the other sampled groups of populations. Our data suggest that bottleneck events followed by strong influence of genetic drift in the process of the peopling of the Americas may have been determinant factors in delineating the genetic background of present-day South Amerindians. Since no clear subgroups were detected within Native Americans and East Asians, there is no indication of multiple waves in the early colonization of the New World.     

Demographic History of Indigenous Populations in Mesoamerica Based on mtDNA Sequence Data

The genetic characterization of Native American groups provides insights into their history and demographic events. We sequenced the mitochondrial D-loop region (control region) of 520 samples from eight Mexican indigenous groups. In addition to an analysis of the genetic diversity, structure and genetic relationship between 28 Native American populations, we applied Bayesian skyline methodology for a deeper insight into the history of Mesoamerica. AMOVA tests applying cultural, linguistic and geographic criteria were performed. MDS plots showed a central cluster of Oaxaca and Maya populations, whereas those from the North and West were located on the periphery. Demographic reconstruction indicates higher values of the effective number of breeding females (Nef) in Central Mesoamerica during the Preclassic period, whereas this pattern moves toward the Classic period for groups in the North and West. Conversely, Nef minimum values are distributed either in the Lithic period (i.e. founder effects) or in recent periods (i.e. population declines). The Mesomerican regions showed differences in population fluctuation as indicated by the maximum Inter-Generational Rate (IGRmax): i) Center-South from the lithic period until the Preclassic; ii) West from the beginning of the Preclassic period until early Classic; iii) North characterized by a wide range of temporal variation from the Lithic to the Preclassic. Our findings are consistent with the genetic variations observed between central, South and Southeast Mesoamerica and the North-West region that are related to differences in genetic drift, structure, and temporal survival strategies (agriculture versus hunter-gathering, respectively). Interestingly, although the European contact had a major negative demographic impact, we detect a previous decline in Mesoamerica that had begun a few hundred years before.     

Hierarchical modeling of genome‐wide Short Tandem Repeat (STR) markers infers native American prehistory

This study examines a genome‐wide dataset of 678 Short Tandem Repeat loci characterized in 444 individuals representing 29 Native American populations as well as the Tundra Netsi and Yakut populations from Siberia. Using these data, the study tests four current hypotheses regarding the hierarchical distribution of neutral genetic variation in native South American populations: (1) the western region of South America harbors more variation than the eastern region of South America, (2) Central American and western South American populations cluster exclusively, (3) populations speaking the Chibchan‐Paezan and Equatorial‐Tucanoan language stock emerge as a group within an otherwise South American clade, (4) Chibchan‐Paezan populations in Central America emerge together at the tips of the Chibchan‐Paezan cluster. This study finds that hierarchical models with the best fit place Central American populations, and populations speaking the Chibchan‐Paezan language stock, at a basal position or separated from the South American group, which is more consistent with a serial founder effect into South America than that previously described. Western (Andean) South America is found to harbor similar levels of variation as eastern (Equatorial‐Tucanoan and Ge‐Pano‐Carib) South America, which is inconsistent with an initial west coast migration into South America. Moreover, in all relevant models, the estimates of genetic diversity within geographic regions suggest a major bottleneck or founder effect occurring within the North American subcontinent, before the peopling of Central and South America. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

High levels of Y-chromosome differentiation among native Siberian populations and the genetic signature of a boreal hunter-gatherer way of life

We examined genetic variation on the nonrecombining portion of the Y chromosome (NRY) to investigate the paternal population structure of indigenous Siberian groups and to reconstruct the historical events leading to the peopling of Siberia. A set of 62 biallelic markers on the NRY were genotyped in 1432 males representing 18 Siberian populations, as well as nine populations from Central and East Asia and one from European Russia. A subset of these markers defines the 18 major NRY haplogroups (A-R) recently described by the Y Chromosome Consortium (YCC 2002). While only four of these 18 major NRY haplogroups accounted for -95% of Siberian Y-chromosome variation, native Siberian populations differed greatly in their haplogroup composition and exhibited the highest phiST value for any region of the world. When we divided our Siberian sample into four geographic regions versus five major linguistic groupings, analyses of molecular variance (AMOVA) indicated higher phiST and phiCT values for linguistic groups than for geographic groups. Mantel tests also supported the existence of NRY genetic patterns that were correlated with language, indicating that language affiliation might be a better predictor of the genetic affinity among Siberians than their present geographic position. The combined results, including those from a nested cladistic analysis, underscored the important role of directed dispersals, range expansions, and long-distance colonizations bound by common ethnic and linguistic affiliation in shaping the genetic landscape of Siberia. The Siberian pattern of reduced haplogroup diversity within populations combined with high levels of differentiation among populations may be a general feature characteristic of indigenous groups that have small effective population sizes and that have been isolated for long periods of time.     

Continent-Wide Decoupling of Y-Chromosomal Genetic Variation from Language and Geography in Native South Americans

Numerous studies of human populations in Europe and Asia have revealed a concordance between their extant genetic structure and the prevailing regional pattern of geography and language. For native South Americans, however, such evidence has been lacking so far. Therefore, we examined the relationship between Y-chromosomal genotype on the one hand, and male geographic origin and linguistic affiliation on the other, in the largest study of South American natives to date in terms of sampled individuals and populations. A total of 1,011 individuals, representing 50 tribal populations from 81 settlements, were genotyped for up to 17 short tandem repeat (STR) markers and 16 single nucleotide polymorphisms (Y-SNPs), the latter resolving phylogenetic lineages Q and C. Virtually no structure became apparent for the extant Y-chromosomal genetic variation of South American males that could sensibly be related to their inter-tribal geographic and linguistic relationships. This continent-wide decoupling is consistent with a rapid peopling of the continent followed by long periods of isolation in small groups. Furthermore, for the first time, we identified a distinct geographical cluster of Y-SNP lineages C-M217 (C3*) in South America. Such haplotypes are virtually absent from North and Central America, but occur at high frequency in Asia. Together with the locally confined Y-STR autocorrelation observed in our study as a whole, the available data therefore suggest a late introduction of C3* into South America no more than 6,000 years ago, perhaps via coastal or trans-Pacific routes. Extensive simulations revealed that the observed lack of haplogroup C3* among extant North and Central American natives is only compatible with low levels of migration between the ancestor populations of C3* carriers and non-carriers. In summary, our data highlight the fact that a pronounced correlation between genetic and geographic/cultural structure can only be expected under very specific conditions, most of which are likely not to have been met by the ancestors of native South Americans.     

Patterns of genetic variation in Native America.

Allele frequencies from seven polymorphic red cell antigen loci (ABO, Rh, MN, S, P, Duffy, and Diego) were examined in 144 Native American populations. Mean genetic distances (Nei's D) and the fixation index FST are approximately equal for the North and South American samples but are reduced in the Central American geographic area. The relationship between genetic distance and geographic distance differs markedly across geographic areas. The correlation between geographic distance and genetic distance for the North and Central American data is twice as large as that observed for the South American samples. This geographic difference is confirmed in spatial autocorrelation analyses; no geographic structure is apparent in the South American data but geographic structure is prominent in North and Central American samples. These results confirm earlier observations regarding differences between North and South American gene frequency patterns.     

A private allele ubiquitous in the Americas

The three-wave migration hypothesis of Greenberg et al. has permeated the genetic literature on the peopling of the Americas. Greenberg et al. proposed that Na-Dene, Aleut-Eskimo and Amerind are language phyla which represent separate migrations from Asia to the Americas. We show that a unique allele at autosomal microsatellite locus D9S1120 is present in all sampled North and South American populations, including the Na-Dene and Aleut-Eskimo, and in related Western Beringian groups, at an average frequency of 31.7%. This allele was not observed in any sampled putative Asian source populations or in other worldwide populations. Neither selection nor admixture explains the distribution of this regionally specific marker. The simplest explanation for the ubiquity of this allele across the Americas is that the same founding population contributed a large fraction of ancestry to all modern Native American populations.     

Native American mtDNA prehistory in the American Southwest

This study examines the mtDNA diversity of the proposed descendants of the multiethnic Hohokam and Anasazi cultural traditions, as well as Uto-Aztecan and Southern-Athapaskan groups, to investigate hypothesized migrations associated with the Southwest region. The mtDNA haplogroups of 117 Native Americans from southwestern North America were determined. The hypervariable segment I (HVSI) portion of the control region of 53 of these individuals was sequenced, and the within-haplogroup diversity of 18 Native American populations from North, Central, and South America was analyzed. Within North America, populations in the West contain higher amounts of diversity than in other regions, probably due to a population expansion and high levels of gene flow among subpopulations in this region throughout prehistory. The distribution of haplogroups in the Southwest is structured more by archaeological tradition than by language. Yumans and Pimans exhibit substantially greater genetic diversity than the Jemez and Zuni, probably due to admixture and genetic isolation, respectively. We find no evidence of a movement of mtDNA lineages northward into the Southwest from Central Mexico, which, in combination with evidence from nuclear markers, suggests that the spread of Uto-Aztecan was facilitated by predominantly male migration. Southern Athapaskans probably experienced a bottleneck followed by extensive admixture during the migration to their current homeland in the Southwest.     

Contrasting the ancestry patterns of three distinct population groups from the northernmost region of South America

Colombia, located in the north of the South American subcontinent is a country of great interest for population genetic studies given its high ethnic and cultural diversity represented by the admixed population, 102 indigenous peoples and African descent populations. In this study, an analysis of the genetic structure and ancestry was performed based on 46 ancestry informative INDEL markers (AIM-INDELs) and considering the genealogical and demographic variables of 451 unrelated individuals belonging to nine Native American, two African American, and four multiple ancestry populations. Measures of genetic diversity, ancestry components, and genetic substructure were analyzed to build a population model typical of the northernmost part of the South American continent. The model suggests three types of populations: Native American, African American, and multiple ancestry. The results support hypotheses posed by other authors about issues like the peopling of South America and the existence of two types of Native American ancestry. This last finding could be crucial for future research on the peopling of Colombia and South America in that a single origin of all indigenous communities should not be assumed. It then would be necessary to consider other events that could explain their genetic variability and complexity throughout the continent.     

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.     

Geographic structure in Gran Chaco Amerindians based on five X-chromosome STRs

We investigated the genetic differentiation of five X-chromosome STR markers among five native South American Amerindian populations inhabiting three different areas of the Gran Chaco: Mocoví, Chorote, Wichí, Lengua, and Ayoreo. The observed genetic structure showed correspondence with geographic distribution more clearly than previous information obtained from autosomal STRs for the same samples. On the other hand, X-chromosome STR data did not agree with linguistic affinities. These markers proved to be informative for the study of the native populations of the Gran Chaco region.     

Y-chromosome diversity in Native Mexicans reveals continental transition of genetic structure in the Americas

The genetic characterization of Native Mexicans is important to understand multiethnic based features influencing the medical genetics of present Mexican populations, as well as to the reconstruct the peopling of the Americas. We describe the Y-chromosome genetic diversity of 197 Native Mexicans from 11 populations and 1,044 individuals from 44 Native American populations after combining with publicly available data. We found extensive heterogeneity among Native Mexican populations and ample segregation of Q-M242* (46%) and Q-M3 (54%) haplogroups within Mexico. The northernmost sampled populations falling outside Mesoamerica (Pima and Tarahumara) showed a clear differentiation with respect to the other populations, which is in agreement with previous results from mtDNA lineages. However, our results point toward a complex genetic makeup of Native Mexicans whose maternal and paternal lineages reveal different narratives of their population history, with sex-biased continental contributions and different admixture proportions. At a continental scale, we found that Arctic populations and the northernmost groups from North America cluster together, but we did not find a clear differentiation within Mesoamerica and the rest of the continent, which coupled with the fact that the majority of individuals from Central and South American samples are restricted to the Q-M3 branch, supports the notion that most Native Americans from Mesoamerica southwards are descendants from a single wave of migration. This observation is compatible with the idea that present day Mexico might have constituted an area of transition in the diversification of paternal lineages during the colonization of the Americas.     

The oriental fruit fly, Bactrocera dorsalis, in China: origin and gradual inland range expansion associated with population growth

The oriental fruit fly, Bactrocera dorsalis, expanded throughout mainland China in the last century to become one of the most serious pests in the area, yet information on this process are fragmentary. Three mitochondrial genes (nad1, cytb and nad5) were used to infer the genetic diversity, population structure and demographic history of the oriental fruit fly from its entire distribution range in China. High levels of genetic diversity, as well as a significant correspondence between genetic and geographic distances, suggest that the invasion process might have been gradual, with no associated genetic bottlenecks. Three population groups could be identified, nevertheless the overall genetic structure was weak. The effective number of migrants between populations, estimated using the coalescent method, suggested asymmetric gene flow from the costal region of Guangdong to most inland regions. The demographic analysis indicates the oriental fruit fly underwent a recent population expansion in the Central China. We suggest the species originated in the costal region facing the South China Sea and gradually expanded to colonize mainland China, expanding here to high population numbers.