Genetic Differentiation in South Amerindians Is Related to Environmental and Cultural Diversity: Evidence from the Y Chromosome

The geographic structure of Y-chromosome variability has been analyzed in native populations of South America, through use of the high-frequency Native American haplogroup defined by the DYS199-T allele and six Y-chromosome–linked microsatellites (DYS19, DYS389A, DYS389B, DYS390, DYS391, and DYS393), analyzed in 236 individuals. The following pattern of within- and among-population variability emerges from the analysis of microsatellite data: (1) the Andean populations exhibit significantly higher levels of within-population variability than do the eastern populations of South America; (2) the spatial-autocorrelation analysis suggests a significant geographic structure of Y-chromosome genetic variability in South America, although a typical evolutionary pattern could not be categorically identified; and (3) genetic-distance analyses and the analysis of molecular variance suggest greater homogeneity between Andean populations than between non-Andean ones. On the basis of these results, we propose a model for the evolution of the male lineages of South Amerindians that involves differential patterns of genetic drift and gene flow. In the western part of the continent, which is associated with the Andean area, populations have relatively large effective sizes and gene-flow levels among them, which has created a trend toward homogenization of the gene pool. On the other hand, eastern populations—settled in the Amazonian region, the central Brazilian plateau, and the Chaco region—have exhibited higher rates of genetic drift and lower levels of gene flow, with a resulting trend toward genetic differentiation. This model is consistent with the linguistic and cultural diversity of South Amerindians, the environmental heterogeneity of the continent, and the available paleoecological data.

PDF file

African-derived South American Populations: A History of Symmetrical and Asymmetrical Matings According to Sex Revealed by Bi- and Uni-parental Genetic Markers

Estimates of African, European, and Amerindian contributions to the gene pool of 11 predominantly African-derived South American populations were obtained using five autosomal and one Y chromosome hypervariable loci, as well as mitochondrial DNA (sequences of the first hypervariable segment of the control region, plus two restriction sites and the presence or absence of the CoII/tRNALys intergenic 9-bp deletion). The three latter characteristics are reported here for the first time for 42 individuals living in three Brazilian populations. Thirty-eight sequences were identified in these persons; 17 (45%) could be classified as being of African, 4 (11%) of Amerindian, and 2 (5%) of European origin. Evidence for asymmetrical matings in relation to sex and ethnic group was obtained for nine of the 11 populations. The most consistent finding was the introduction of European genes through males, but the results differ in the several communities, indicating the importance of local factors in such interactions.

PDF file

ANALYSES OF DNA FROM ANCIENT BONES OF A PRE-COLUMBIAN CUBAN WOMAN AND A CHILD

Molecular anthropology has brought new possibilities into the study of ancient human populations. Amplification of chromosomal short tandem repeat (STR) loci and mitochondrial DNA (mtDNA) has been successfully employed in analyses of ancient bone material. Although several studies have reported on continental Amerindian populations, none have addressed the ancient populations inhabiting the Caribbean islands. We used STR and mtDNA analyses to study the skeletal remains of a Cuban Ciboney female adult holding an infant. Results showed that for the STR analyzed the skeletal remains shared common alleles, suggesting a relationship. Mitochondrial DNA analysis showed sequence identity, thus corroborating a possible mother-child relationship. The mtDNA sequence grouped these remains into haplogroup A, commonly found in Amerindian populations. Based on these results, we speculated on a South American origin of pre-Columbian Antilles populations and possible infanticide practices in these populations. This constitutes the first report on DNA analysis of ancient pre-Columbian Cuban populations.

PDF file

Genetic approaches to understanding human adaptation to altitude in the Andes

Despite the initial discomfort often experienced by visitors to high-altitude, humans have occupied the Andean altiplano for more than 10 000 years, and millions of people, indigenous and otherwise, currently live on these plains, high in the mountains of South America, at altitudes exceeding 3000 m. While, to some extent, acclimatisation can accommodate the one-third decrease in oxygen availability, having been born and raised at altitude appears to confer a substantial advantage in high altitude performance compared with having been born and raised at sea level. A number of characteristics have been postulated to contribute to a high-altitude Andean phenotype; however, the relative contributions of developmental adaptation (within the individual) and genetic adaptation (within the population of which the individual is part) to the acquisition of this phenotype have yet to be resolved. A complex trait is influenced by multiple genetic and environmental factors and, in humans, it is inherently very difficult to determine what proportion of the trait is dictated by an individual’s genetic heritage and what proportion develops in response to the environment in which the person is born and raised. Looking for changes in putative adaptations in vertically migrant populations, determining the heritability of putative adaptive traits and genetic association analyses have all been used to evaluate the relative contributions of nurture and nature to the Andean phenotype. As the evidence for a genetic contribution to high-altitude adaptation in humans has been the subject of several recent reviews, this article instead focuses on the methodology that has been employed to isolate the effects of ‘nature’ from those of ‘nurture’ on the acquisition of the high-altitude phenotype in Andean natives (Quechua and Aymara). The principles and assumptions underlying the various approaches, as well as some of the inherent strengths and weaknesses of each, are briefly discussed.

PDF file

Mitochondrial DNA Diversity in South America and the Genetic History of Andean Highlanders

We analyzed mtDNA sequence variation in 590 individuals from 18 south Amerindian populations. The spatial pattern of mtDNA diversity in these populations fits well the model proposed on the basis of Y-chromosome data. We found evidence of a differential action of genetic drift and gene flow in western and eastern populations, which has led to genetic divergence in the latter but not in the former. Although it is not possible to identify a pattern of genetic variation common to all South America, when western and eastern populations are analyzed separately, the mtDNA diversity in both regions fits the isolation-by-distance model, suggesting independent evolutionary dynamics. Maximum-likelihood estimates of divergence times between central and south Amerindian populations fall between 13,000 and 19,000 years, which is consistent with a Pleistocenic peopling of South America. Moreover, comparison of among-population variability of mtDNA and Y-chromosome DNA seems to indicate that South America is the only continent where the levels of differentiation are similar for maternal and paternal lineages.

PDF file

The Peopling of the Pacific

Archaeologists, linguists, and geneticists struggle to understand the origins of the bold seafarers who settled the remote Pacific Islands.

PDF file

Origins and dispersals of Pacific peoples: Evidence from mtDNA phylogenies of the Pacific rat

The human settlement of the Pacific in general, and the origin of the Polynesians in particular, have been topics of debate for over two centuries. Polynesian origins are most immediately traced to people who arrived in the Fiji, Tonga, and Samoa region ~3,000 B.P. and are clearly associated with the Lapita Cultural Complex. Although this scenario of the immediate origins of the Polynesians is generally accepted, the debate on the ultimate origin of the Polynesians and the Lapita cultural complex continues. Our previous research has shown that analyses of mtDNA variation in the Pacific rat (Rattus exulans), often transported as a food item in the colonizing canoes, are valuable for tracing prehistoric human migration within Polynesia. Here we present mtDNA phylogenies based on ~240 base pairs of the D-loop from both archaeological and modern samples collected from Island Southeast Asia and the Pacific. We identify three major haplogroups, two of which occur in the Pacific. Comparing our results with Lapita models of Oceanic settlement, we are able to reject two often cited but simplistic models, finding support instead for multifaceted models incorporating a more complex view of the Lapita intrusion. This study is unique and valuable in that R. exulans is the only organism associated with the Lapita dispersal for which there are sufficient ancient and extant populations available for genetic analysis. By tracking population changes through time, we can understand more fully the settlement process and population interactions in both Near and Remote Oceania.

PDF file

Mitochondrial lineages in Ladin-speaking communities of the eastern Alps

European mitochondrial alleles cluster into five haplogroups. Haplogroup 2 is rare in general, but represents more than half of the few known sequences among Ladin speakers of the Alps. Here we describe DNA diversity in control region I of the hypervariable D-loop in 43 Ladins, and in 25 Italian speakers. Analysis of these data, and of previously published sequences, confirms a high degree of differentiation among Ladins and their geographical neighbours. This cannot be regarded as a simple effect of isolating factors, geographic or linguistic, as diversity is high within Ladin communities too. Rather, allele genealogies, population trees, and principal component analysis suggest a relationship between Ladin and Near Eastern samples. Two evolutionary hypotheses seem compatible with these findings. The view whereby Ladins could be descended from Palaeolithic inhabitants of the Alps is supported by the identification, in this study, of the probable ancestral haplotype of group 2, never previously observed in central Europe. Alternatively, a comparatively recent, Neolithic immigration of the ancestors of current Ladin speakers seems consistent with recent linguistic theories. In both cases, the number of lineages present, and their extensive diversity, are not compatible with a serious bottleneck in the Ladin population's history.

PDF file

Mitochondrial Diversity in Linguistic Isolates of the Alps: A Reappraisal

In Stenico et al. (1996) we reported unusually high levels of mitochondrial diversity in the Alps. In particular, two communities of Ladin speakers appeared the most extreme European mitochondrial outliers at that time. Recently, it has been observed that some rare nucleotide substitutions occur repeatedly among those sequences, raising the possibility of systematic sequencing errors. No biological material was left from the previous study, and hence we had to sample new individuals from the same communities. Here, we present the HVSI sequence variation, along with haplogroup assignment based on restriction fragment length polymorphism (RFLP), in 20 Ladin speakers of Colle Santa Lucia. None of the new sequences displays substitutions at the sites viewed as problematic. However, Ladins still show high levels of mtDNA diversity, both within their community and with respect to other Europeans, and they can still be considered one of the main European mitochondrial outliers.

PDF file

The Genetic Legacy of Paleolithic Homo sapiens sapiens in Extant Europeans: A Y Chromosome Perspective

A genetic perspective of human history in Europe was derived from 22 binary markers of the nonrecombining Y chromosome (NRY). Ten lineages account for >95% of the 1007 European Y chromosomes studied. Geographic distribution and age estimates of alleles are compatible with two Paleolithic and one Neolithic migratory episode that have contributed to the modern European gene pool. A significant correlation between the NRY haplotype data and principal components based on 95 protein markers was observed, indicating the effectiveness of NRY binary polymorphisms in the characterization of human population composition and history.

PDF file

AFRICANS AND ASIANS ABROAD: Genetic Diversity in Europe

Besides its obvious intrinsic value, knowledge of population history, and of the demographic and evolutionary changes that accompany it, has proven fundamental to address applied research in human genetics. In this review we place current European genetic diversity in the context of the global human genome diversity and review the evidence supporting a recent African origin of the Europeans. We then discuss the results and the interpretation of genetic studies attempting to quantify the relative importance of various gene flow processes, both within Europe and from Asia into Europe, focusing especially on the initial, Paleolithic colonization of the continent, and on later, Paleolithic postglacial and Neolithic dispersals. Finally, we discuss how knowledge of the patterns of genetic diversity in Europe, and of their inferred generating processes, can be extremely useful in planning health care and in biomedical research.

PDF file

A Predominantly Indigenous Paternal Heritage for the Austronesian-Speaking Peoples of Insular Southeast Asia and Oceania

Modern humans reached Southeast Asia and Oceania in one of the first dispersals out of Africa. The resulting temporal overlap of modern and archaic humans—and the apparent morphological continuity between them—has led to claims of gene flow between Homo sapiens and H. erectus. Much more recently, an agricultural technology from mainland Asia spread into the region, possibly in association with Austronesian languages. Using detailed genealogical study of Y chromosome variation, we show that the majority of current Austronesian speakers trace their paternal heritage to Pleistocene settlers in the region, as opposed to more-recent agricultural immigrants. A fraction of the paternal heritage, however, appears to be associated with more-recent immigrants from northern populations. We also show that the northern Neolithic component is very unevenly dispersed through the region, with a higher contribution in Southeast Asia and a nearly complete absence in Melanesia. Contrary to claims of gene flow (under regional continuity) between H. erectus and H. sapiens, we found no ancestral Y chromosome lineages in a set of 1,209 samples. The finding excludes the possibility that early hominids contributed significantly to the paternal heritage of the region.

PDF file

Genetic Evidence for the Proto-Austronesian Homeland in Asia: mtDNA and Nuclear DNA Variation in Taiwanese Aboriginal Tribes

Previous studies of mtDNA variation in indigenous Taiwanese populations have suggested that they held an ancestral position in the spread of mtDNAs throughout Southeast Asia and Oceania (Melton et al. 1995; Sykes et al. 1995), but the question of an absolute proto-Austronesian homeland remains. To search for Asian roots for indigenous Taiwanese populations, 28 mtDNAs representative of variation in four tribal groups (Ami, Atayal, Bunun, and Paiwan) were sequenced and were compared with each other and with mtDNAs from 25 other populations from Asia and Oceania. In addition, eight polymorphic Alu insertion loci were analyzed, to determine if the pattern of mtDNA variation is concordant with nuclear DNA variation. Tribal groups shared considerable mtDNA sequence identity (P>.90), where gene flow is believed to have been low, arguing for a common source or sources for the tribes. mtDNAs with a 9-bp deletion have considerable mainland-Asian diversity and have spread to Southeast Asia and Oceania through a Taiwanese bottleneck. Only four Taiwanese mtDNA haplotypes without the 9-bp deletion were shared with any other populations, but these shared types were widely dispersed geographically throughout mainland Asia. Phylogenetic and principal-component analyses of Alu loci were concordant with conclusions from the mtDNA analyses; overall, the results suggest that the Taiwanese have temporally deep roots, probably in central or south China, and have been isolated from other Asian populations in recent history.

PDF file

Y Chromosomal Evidence for the Origins of Oceanic-Speaking Peoples

A number of alternative hypotheses seek to explain the origins of the three groups of Pacific populations—Melanesians, Micronesians, and Polynesians—who speak languages belonging to the Oceanic subfamily of Austronesian languages. To test these various hypotheses at the genetic level, we assayed diversity within the nonrecombining portion of the Y chromosome, which contains within it a relatively simple record of the human past and represents the most informative haplotypic system in the human genome. High-resolution haplotypes combining binary, microsatellite, and minisatellite markers were generated for 390 Y chromosomes from 17 Austronesian-speaking populations in southeast Asia and the Pacific. Nineteen paternal lineages were defined and a Bayesian analysis of coalescent simulations was performed upon the microsatellite diversity within lineages to provide a temporal aspect to their geographical distribution. The ages and distributions of these lineages provide little support for the dominant archeo-linguistic model of the origins of Oceanic populations that suggests that these peoples represent the Eastern fringe of an agriculturally driven expansion initiated in southeast China and Taiwan. Rather, most Micronesian and Polynesian Y chromosomes appear to originate from different source populations within Melanesia and Eastern Indonesia. The Polynesian outlier, Kapingamarangi, is demonstrated to be an admixed Micronesian/Polynesian population. Furthermore, it is demonstrated that a geographical rather than linguistic classification of Oceanic populations best accounts for their extant Y chromosomal diversity.

PDF file

Fast trains, slow boats, and the ancestry of the Polynesian islanders

PDF file

The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations

Although molecular genetic evidence continues to accumulate that is consistent with a recent common African ancestry of modern humans, its ability to illuminate regional histories remains incomplete. A set of unique event polymorphisms associated with the non-recombining portion of the Y-chromosome (NRY) addresses this issue by providing evidence concerning successful migrations originating from Africa, which can be interpreted as subsequent colonizations, differentiations and migrations overlaid upon previous population ranges. A total of 205 markers identified by denaturing high performance liquid chromatography (DHPLC), together with 13 taken from the literature, were used to construct a parsimonious genealogy. Ancestral allelic states were deduced from orthologous great ape sequences. A total of 131 unique haplotypes were defined which trace the microevolutionary trajectory of global modern human genetic diversification. The genealogy provides a detailed phylogeographic portrait of contemporary global population structure that is emblematic of human origins, divergence and population history that is consistent with climatic, paleoanthropological and other genetic knowledge.

PDF file

Origins of modern humans still look recent

PDF file

The Levant versus the Horn of Africa: Evidence for Bidirectional Corridors of Human Migrations

Paleoanthropological evidence indicates that both the Levantine corridor and the Horn of Africa served, repeatedly, as migratory corridors between Africa and Eurasia. We have begun investigating the roles of these passageways in bidirectional migrations of anatomically modern humans, by analyzing 45 informative biallelic markers as well as 10 microsatellite loci on the nonrecombining region of the Y chromosome (NRY) in 121 and 147 extant males from Oman and northern Egypt, respectively. The present study uncovers three important points concerning these demic movements: (1) The E3b1-M78 and E3b3-M123 lineages, as well as the R1*-M173 lineages, mark gene flow between Egypt and the Levant during the Upper Paleolithic and Mesolithic. (2) In contrast, the Horn of Africa appears to be of minor importance in the human migratory movements between Africa and Eurasia represented by these chromosomes, an observation based on the frequency distributions of E3b*-M35 (no known downstream mutations) and M173. (3) The areal diffusion patterns of G-M201, J-12f2, the derivative M173 haplogroups, and M2 suggest more recent genetic associations between the Middle East and Africa, involving the Levantine corridor and/or Arab slave routes. Affinities to African groups were also evaluated by determining the NRY haplogroup composition in 434 samples from seven sub-Saharan African populations. Oman and Egypt’s NRY frequency distributions appear to be much more similar to those of the Middle East than to any sub-Saharan African population, suggesting a much larger Eurasian genetic component. Finally, the overall phylogeographic profile reveals several clinal patterns and genetic partitions that may indicate source, direction, and relative timing of different waves of dispersals and expansions involving these nine populations.

PDF file

Errata

Y chromosomal haplogroup J as a signature of the post-neolithic colonization of Europe

In order to attain a finer reconstruction of the peopling of southern and central-eastern Europe from the Levant, we determined the frequencies of eight lineages internal to the Y chromosomal haplogroup J, defined by biallelic markers, in 22 population samples obtained with a fine-grained sampling scheme. Our results partially resolve a major multifurcation of lineages within the haplogroup. Analyses of molecular variance show that the area covered by haplogroup J dispersal is characterized by a significant degree of molecular radiation for unique event polymorphisms within the haplogroup, with a higher incidence of the most derived sub-haplogroups on the northern Mediterranean coast, from Turkey westward; here, J diversity is not simply a subset of that present in the area in which this haplogroup first originated. Dating estimates, based on simple tandem repeat loci (STR) diversity within each lineage, confirmed the presence of a major population structuring at the time of spread of haplogroup J in Europe and a punctuation in the peopling of this continent in the post-Neolithic, compatible with the expansion of the Greek world. We also present here, for the first time, a novel method for comparative dating of lineages, free of assumptions of STR mutation rates.

PDF file

Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa

The out-of-Africa scenario has hitherto provided little evidence for the precise route by which modern humans left Africa. Two major routes of dispersal have been hypothesized: one through North Africa into the Levant, documented by fossil remains, and one through Ethiopia along South Asia, for which little, if any, evidence exists. Mitochondrial DNA (mtDNA) can be used to trace maternal ancestry. The geographic distribution and variation of mtDNAs can be highly informative in defining potential range expansions and migration routes in the distant past. The mitochondrial haplogroup M, first regarded as an ancient marker of East-Asian origin, has been found at high frequency in India and Ethiopia, raising the question of its origin. (A haplogroup is a group of haplotypes that share some sequence variations.) Its variation and geographical distribution suggest that Asian haplogroup M separated from eastern-African haplogroup M more than 50,000 years ago. Two other variants (489C and 10873C) also support a single origin of haplogroup M in Africa. These findings, together with the virtual absence of haplogroup M in the Levant and its high frequency in the South-Arabian peninsula, render M the first genetic indicator for the hypothesized exit route from Africa through eastern Africa/western India. This was possibly the only successful early dispersal event of modern humans out of Africa.

PDF file

Phylogenetic Network for European mtDNA

The sequence in the first hypervariable segment (HVS-I) of the control region has been used as a source of evolutionary information in most phylogenetic analyses of mtDNA. Population genetic inference would benefit from a better understanding of the variation in the mtDNA coding region, but, thus far, complete mtDNA sequences have been rare. We determined the nucleotide sequence in the coding region of mtDNA from 121 Finns, by conformation-sensitive gel electrophoresis and subsequent sequencing and by direct sequencing of the D loop. Furthermore, 71 sequences from our previous reports were included, so that the samples represented all the mtDNA haplogroups present in the Finnish population. We found a total of 297 variable sites in the coding region, which allowed the compilation of unambiguous phylogenetic networks. The D loop harbored 104 variable sites, and, in most cases, these could be localized within the coding-region networks, without discrepancies. Interestingly, many homoplasies were detected in the coding region. Nucleotide variation in the rRNA and tRNA genes was 6%, and that in the third nucleotide positions of structural genes amounted to 22% of that in the HVS-I. The complete networks enabled the relationships between the mtDNA haplogroups to be analyzed. Phylogenetic networks based on the entire coding-region sequence in mtDNA provide a rich source for further population genetic studies, and complete sequences make it easier to differentiate between disease-causing mutations and rare polymorphisms.

PDF file

mtDNA Haplogroups and Frequency Patterns in Europe

PDF file