Genomic evidence for shared common ancestry of East African hunting-gathering populations and insights into local adaptation

Contributed by Sarah A. Tishkoff, January 5, 2019 (sent for review October 15, 2018; reviewed by Rob J. Kulathinal and Mark D. Shriver)
February 19, 2019
116 (10) 4166-4175

Significance

African populations have been underrepresented in human genomics research yet are important for understanding modern human origins and the genetic basis of adaptive traits. Here we analyze a genome-wide dataset in 840 ethnically and geographically diverse Africans. We find that geographically distant hunter-gatherer populations from East Africa share unique common ancestry and we see strong signatures of local adaptation near genes that play a role in immune response, as well as lipid and glucose metabolism.

Abstract

Anatomically modern humans arose in Africa ∼300,000 years ago, but the demographic and adaptive histories of African populations are not well-characterized. Here, we have generated a genome-wide dataset from 840 Africans, residing in western, eastern, southern, and northern Africa, belonging to 50 ethnicities, and speaking languages belonging to four language families. In addition to agriculturalists and pastoralists, our study includes 16 populations that practice, or until recently have practiced, a hunting-gathering (HG) lifestyle. We observe that genetic structure in Africa is broadly correlated not only with geography, but to a lesser extent, with linguistic affiliation and subsistence strategy. Four East African HG (EHG) populations that are geographically distant from each other show evidence of common ancestry: the Hadza and Sandawe in Tanzania, who speak languages with clicks classified as Khoisan; the Dahalo in Kenya, whose language has remnant clicks; and the Sabue in Ethiopia, who speak an unclassified language. Additionally, we observed common ancestry between central African rainforest HGs and southern African San, the latter of whom speak languages with clicks classified as Khoisan. With the exception of the EHG, central African rainforest HGs, and San, other HG groups in Africa appear genetically similar to neighboring agriculturalist or pastoralist populations. We additionally demonstrate that infectious disease, immune response, and diet have played important roles in the adaptive landscape of African history. However, while the broad biological processes involved in recent human adaptation in Africa are often consistent across populations, the specific loci affected by selective pressures more often vary across populations.

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Data Availability

Data deposition: Genotype data from this study have been deposited in the NIH dbGAP repository, https://www.ncbi.nlm.nih.gov/gap (accession no. phs001780.v1.p1).

Acknowledgments

We thank Joseph Lachance for helpful comments and discussion; and the African volunteers for samples. Genotyping services were provided by Hakon Hakonarsson of the Center for Applied Genomics at the Children’s Hospital of Philadelphia. This research was funded by National Science Foundation Grants BCS-0196183 and BCS-0827436 and National Institutes of Health Grants 8DP1ES022577, 5-R01-GM076637, 1R01DK104339, and 1R01GM113657 (to S.A.T.).

Supporting Information

Appendix (PDF)
Dataset_S01 (CSV)
Dataset_S02 (CSV)
Dataset_S03 (CSV)

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Information & Authors

Information

Published in

The cover image for PNAS Vol.116; No.10
Proceedings of the National Academy of Sciences
Vol. 116 | No. 10
March 5, 2019
PubMed: 30782801

Classifications

Data Availability

Data deposition: Genotype data from this study have been deposited in the NIH dbGAP repository, https://www.ncbi.nlm.nih.gov/gap (accession no. phs001780.v1.p1).

Submission history

Published online: February 19, 2019
Published in issue: March 5, 2019

Keywords

  1. African hunter-gatherers
  2. African diversity
  3. population genetics
  4. natural selection
  5. human evolution

Acknowledgments

We thank Joseph Lachance for helpful comments and discussion; and the African volunteers for samples. Genotyping services were provided by Hakon Hakonarsson of the Center for Applied Genomics at the Children’s Hospital of Philadelphia. This research was funded by National Science Foundation Grants BCS-0196183 and BCS-0827436 and National Institutes of Health Grants 8DP1ES022577, 5-R01-GM076637, 1R01DK104339, and 1R01GM113657 (to S.A.T.).

Authors

Affiliations

Laura B. Scheinfeldt1
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Present address: Coriell Institute for Medical Research, Camden, NJ 08103.
Sameer Soi1
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Genomics and Computational Biology Graduate Program, University of Pennsylvania, Philadelphia, PA 19104;
Charla Lambert
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Present address: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724.
Wen-Ya Ko
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Present address: Department of Life Sciences and Institute of Genome Sciences, National Yang Ming University, Taipei City 112, Taiwan.
Aoua Coulibaly
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Alessia Ranciaro
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Simon Thompson
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Jibril Hirbo
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Present address: Division of Genetic Medicine, Vanderbilt University Medical Center, Vanderbilt University, Nashville, TN 37232.
William Beggs
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Muntaser Ibrahim
Department of Molecular Biology, Institute of Endemic Diseases, University of Khartoum, Khartoum, Sudan;
Thomas Nyambo
Department of Biochemistry, St. Joseph University College of Health Sciences, Dar es Salaam, Tanzania;
Sabah Omar
Kenya Medical Research Institute, Center for Biotechnology Research and Development, Nairobi, Kenya;
Dawit Woldemeskel
Department of Biology, Addis Ababa University, Addis Ababa, Ethiopia;
Gurja Belay
Department of Biology, Addis Ababa University, Addis Ababa, Ethiopia;
Alain Froment
UMR 208, Institut de Recherche pour le Développement-Muséum National d’Histoire Naturelle, Musée de l’Homme, 75116 Paris, France;
Junhyong Kim
Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104
Sarah A. Tishkoff6 [email protected]
Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104

Notes

6
To whom correspondence should be addressed. Email: [email protected].
Author contributions: L.B.S., J.K., and S.A.T. designed research; L.B.S., S.S., W.-Y.K., A.R., S.T., J.H., M.I., T.N., S.O., D.W., G.B., A.F., and S.A.T. performed research; L.B.S., S.S., C.L., A.C., W.B., and S.A.T. analyzed data; and L.B.S., S.S., J.K., and S.A.T. wrote the paper.
Reviewers: R.J.K., Temple University; and M.D.S., Pennsylvania State University.
1
L.B.S. and S.S. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    Genomic evidence for shared common ancestry of East African hunting-gathering populations and insights into local adaptation
    Proceedings of the National Academy of Sciences
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    • pp. 3935-4748

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