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      Early Back-to-Africa Migration into the Horn of Africa

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          Abstract

          Genetic studies have identified substantial non-African admixture in the Horn of Africa (HOA). In the most recent genomic studies, this non-African ancestry has been attributed to admixture with Middle Eastern populations during the last few thousand years. However, mitochondrial and Y chromosome data are suggestive of earlier episodes of admixture. To investigate this further, we generated new genome-wide SNP data for a Yemeni population sample and merged these new data with published genome-wide genetic data from the HOA and a broad selection of surrounding populations. We used multidimensional scaling and ADMIXTURE methods in an exploratory data analysis to develop hypotheses on admixture and population structure in HOA populations. These analyses suggested that there might be distinct, differentiated African and non-African ancestries in the HOA. After partitioning the SNP data into African and non-African origin chromosome segments, we found support for a distinct African (Ethiopic) ancestry and a distinct non-African (Ethio-Somali) ancestry in HOA populations. The African Ethiopic ancestry is tightly restricted to HOA populations and likely represents an autochthonous HOA population. The non-African ancestry in the HOA, which is primarily attributed to a novel Ethio-Somali inferred ancestry component, is significantly differentiated from all neighboring non-African ancestries in North Africa, the Levant, and Arabia. The Ethio-Somali ancestry is found in all admixed HOA ethnic groups, shows little inter-individual variance within these ethnic groups, is estimated to have diverged from all other non-African ancestries by at least 23 ka, and does not carry the unique Arabian lactase persistence allele that arose about 4 ka. Taking into account published mitochondrial, Y chromosome, paleoclimate, and archaeological data, we find that the time of the Ethio-Somali back-to-Africa migration is most likely pre-agricultural.

          Author Summary

          The Horn of Africa (HOA) occupies a central place in our understanding of modern human origins. This region is the location of the earliest known modern human fossils, a possible source for the out-of-Africa migration, and one of the most genetically and linguistically diverse regions of the world. Numerous genetic studies over the last decades have identified substantial non-African ancestry in populations in this region. Because there is archaeological, historical, and linguistic evidence for contact with non-African populations beginning about 3,000 years ago, it has often been assumed that the non-African ancestry in HOA populations dates to this time. In this work, we find that the genetic composition of non-African ancestry in the HOA is distinct from the genetic composition of current populations in North Africa and the Middle East. With these data, we demonstrate that most non-African ancestry in the HOA cannot be the result of admixture within the last few thousand years, and that the majority of admixture probably occurred prior to the advent of agriculture. These results contribute to a growing body of work showing that prehistoric hunter-gatherer populations were much more dynamic than usually assumed.

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          Most cited references39

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          A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase.

          We present a statistical model for patterns of genetic variation in samples of unrelated individuals from natural populations. This model is based on the idea that, over short regions, haplotypes in a population tend to cluster into groups of similar haplotypes. To capture the fact that, because of recombination, this clustering tends to be local in nature, our model allows cluster memberships to change continuously along the chromosome according to a hidden Markov model. This approach is flexible, allowing for both "block-like" patterns of linkage disequilibrium (LD) and gradual decline in LD with distance. The resulting model is also fast and, as a result, is practicable for large data sets (e.g., thousands of individuals typed at hundreds of thousands of markers). We illustrate the utility of the model by applying it to dense single-nucleotide-polymorphism genotype data for the tasks of imputing missing genotypes and estimating haplotypic phase. For imputing missing genotypes, methods based on this model are as accurate or more accurate than existing methods. For haplotype estimation, the point estimates are slightly less accurate than those from the best existing methods (e.g., for unrelated Centre d'Etude du Polymorphisme Humain individuals from the HapMap project, switch error was 0.055 for our method vs. 0.051 for PHASE) but require a small fraction of the computational cost. In addition, we demonstrate that the model accurately reflects uncertainty in its estimates, in that probabilities computed using the model are approximately well calibrated. The methods described in this article are implemented in a software package, fastPHASE, which is available from the Stephens Lab Web site.
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            The genetic structure and history of Africans and African Americans.

            Africa is the source of all modern humans, but characterization of genetic variation and of relationships among populations across the continent has been enigmatic. We studied 121 African populations, four African American populations, and 60 non-African populations for patterns of variation at 1327 nuclear microsatellite and insertion/deletion markers. We identified 14 ancestral population clusters in Africa that correlate with self-described ethnicity and shared cultural and/or linguistic properties. We observed high levels of mixed ancestry in most populations, reflecting historical migration events across the continent. Our data also provide evidence for shared ancestry among geographically diverse hunter-gatherer populations (Khoesan speakers and Pygmies). The ancestry of African Americans is predominantly from Niger-Kordofanian (approximately 71%), European (approximately 13%), and other African (approximately 8%) populations, although admixture levels varied considerably among individuals. This study helps tease apart the complex evolutionary history of Africans and African Americans, aiding both anthropological and genetic epidemiologic studies.
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              Farmers and their languages: the first expansions.

              The largest movements and replacements of human populations since the end of the Ice Ages resulted from the geographically uneven rise of food production around the world. The first farming societies thereby gained great advantages over hunter-gatherer societies. But most of those resulting shifts of populations and languages are complex, controversial, or both. We discuss the main complications and specific examples involving 15 language families. Further progress will depend on interdisciplinary research that combines archaeology, crop and livestock studies, physical anthropology, genetics, and linguistics.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                June 2014
                12 June 2014
                : 10
                : 6
                : e1004393
                Affiliations
                [1 ]Department of Life Sciences, Silwood Park Campus, Imperial College London, Ascot, Berkshire, United Kingdom
                [2 ]Department of Anthropology and the Genetics Institute, University of Florida, Gainesville, Florida, United States of America
                [3 ]Department of Biochemistry and Molecular Biology, Sana'a University, Sana'a, Yemen
                [4 ]Department of Anthropology, Lehman College and The Graduate Center, The City University of New York, Bronx, New York, New York, United States of America
                [5 ]The New York Consortium in Evolutionary Primatology (NYCEP), New York, New York, United States of America
                Dartmouth College, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JAH RLR. Performed the experiments: JAH CJM RLR. Analyzed the data: JAH RLR. Contributed reagents/materials/analysis tools: CJM AAM. Wrote the paper: JAH RLR.

                Article
                PGENETICS-D-13-01333
                10.1371/journal.pgen.1004393
                4055572
                24921250
                147e6546-e650-47fc-b722-e7f05fb0c1f3
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 20 May 2013
                : 7 April 2014
                Page count
                Pages: 18
                Funding
                This work was supported by NSF BCS-0518530 to CJM and by research funds provided by the School of Natural and Social Sciences of Lehman College to RLR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Evolutionary Biology
                Organismal Evolution
                Human Evolution
                Population Genetics
                Gene Flow
                Physical Anthropology
                Social Sciences
                Anthropology

                Genetics
                Genetics

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