Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest

Marie Lopez, Jeremy Choin, Martin Sikora, Katherine Siddle, Christine Harmant, Helio A. Costa, Martin Silvert, Patrick Mouguiama-Daouda, Jean Marie Hombert, Alain Froment, Sylvie Le Bomin, George H. Perry, Luis B. Barreiro, Carlos D. Bustamante, Paul Verdu, Etienne Patin, Lluís Quintana-Murci

Research output: Contribution to journalArticle

Abstract

African rainforests support exceptionally high biodiversity and host the world's largest number of active hunter-gatherers [1–3]. The genetic history of African rainforest hunter-gatherers and neighboring farmers is characterized by an ancient divergence more than 100,000 years ago, together with recent population collapses and expansions, respectively [4–12]. While the demographic past of rainforest hunter-gatherers has been deeply characterized, important aspects of their history of genetic adaptation remain unclear. Here, we investigated how these groups have adapted—through classic selective sweeps, polygenic adaptation, and selection since admixture—to the challenging rainforest environments. To do so, we analyzed a combined dataset of 566 high-coverage exomes, including 266 newly generated exomes, from 14 populations of rainforest hunter-gatherers and farmers, together with 40 newly generated, low-coverage genomes. We find evidence for a strong, shared selective sweep among all hunter-gatherer groups in the regulatory region of TRPS1—primarily involved in morphological traits. We detect strong signals of polygenic adaptation for height and life history traits such as reproductive age; however, the latter appear to result from pervasive pleiotropy of height-associated genes. Furthermore, polygenic adaptation signals for functions related to responses of mast cells to allergens and microbes, the IL-2 signaling pathway, and host interactions with viruses support a history of pathogen-driven selection in the rainforest. Finally, we find that genes involved in heart and bone development and immune responses are enriched in both selection signals and local hunter-gatherer ancestry in admixed populations, suggesting that selection has maintained adaptive variation in the face of recent gene flow from farmers.

Original languageEnglish (US)
Pages (from-to)2926-2935.e4
JournalCurrent Biology
Volume29
Issue number17
DOIs
StatePublished - Sep 9 2019

Fingerprint

rain forests
Genes
genomics
Exome
farmers
Nucleic Acid Regulatory Sequences
Biodiversity
Pathogens
Viruses
Allergens
Population
Interleukin-2
pleiotropy
Bone
skeletal development
Gene Flow
Bone Development
mast cells
allergens
interleukin-2

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Lopez, M., Choin, J., Sikora, M., Siddle, K., Harmant, C., Costa, H. A., ... Quintana-Murci, L. (2019). Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest. Current Biology, 29(17), 2926-2935.e4. https://doi.org/10.1016/j.cub.2019.07.013
Lopez, Marie ; Choin, Jeremy ; Sikora, Martin ; Siddle, Katherine ; Harmant, Christine ; Costa, Helio A. ; Silvert, Martin ; Mouguiama-Daouda, Patrick ; Hombert, Jean Marie ; Froment, Alain ; Le Bomin, Sylvie ; Perry, George H. ; Barreiro, Luis B. ; Bustamante, Carlos D. ; Verdu, Paul ; Patin, Etienne ; Quintana-Murci, Lluís. / Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest. In: Current Biology. 2019 ; Vol. 29, No. 17. pp. 2926-2935.e4.
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Lopez, M, Choin, J, Sikora, M, Siddle, K, Harmant, C, Costa, HA, Silvert, M, Mouguiama-Daouda, P, Hombert, JM, Froment, A, Le Bomin, S, Perry, GH, Barreiro, LB, Bustamante, CD, Verdu, P, Patin, E & Quintana-Murci, L 2019, 'Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest', Current Biology, vol. 29, no. 17, pp. 2926-2935.e4. https://doi.org/10.1016/j.cub.2019.07.013

Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest. / Lopez, Marie; Choin, Jeremy; Sikora, Martin; Siddle, Katherine; Harmant, Christine; Costa, Helio A.; Silvert, Martin; Mouguiama-Daouda, Patrick; Hombert, Jean Marie; Froment, Alain; Le Bomin, Sylvie; Perry, George H.; Barreiro, Luis B.; Bustamante, Carlos D.; Verdu, Paul; Patin, Etienne; Quintana-Murci, Lluís.

In: Current Biology, Vol. 29, No. 17, 09.09.2019, p. 2926-2935.e4.

Research output: Contribution to journalArticle

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AU - Choin, Jeremy

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AU - Silvert, Martin

AU - Mouguiama-Daouda, Patrick

AU - Hombert, Jean Marie

AU - Froment, Alain

AU - Le Bomin, Sylvie

AU - Perry, George H.

AU - Barreiro, Luis B.

AU - Bustamante, Carlos D.

AU - Verdu, Paul

AU - Patin, Etienne

AU - Quintana-Murci, Lluís

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N2 - African rainforests support exceptionally high biodiversity and host the world's largest number of active hunter-gatherers [1–3]. The genetic history of African rainforest hunter-gatherers and neighboring farmers is characterized by an ancient divergence more than 100,000 years ago, together with recent population collapses and expansions, respectively [4–12]. While the demographic past of rainforest hunter-gatherers has been deeply characterized, important aspects of their history of genetic adaptation remain unclear. Here, we investigated how these groups have adapted—through classic selective sweeps, polygenic adaptation, and selection since admixture—to the challenging rainforest environments. To do so, we analyzed a combined dataset of 566 high-coverage exomes, including 266 newly generated exomes, from 14 populations of rainforest hunter-gatherers and farmers, together with 40 newly generated, low-coverage genomes. We find evidence for a strong, shared selective sweep among all hunter-gatherer groups in the regulatory region of TRPS1—primarily involved in morphological traits. We detect strong signals of polygenic adaptation for height and life history traits such as reproductive age; however, the latter appear to result from pervasive pleiotropy of height-associated genes. Furthermore, polygenic adaptation signals for functions related to responses of mast cells to allergens and microbes, the IL-2 signaling pathway, and host interactions with viruses support a history of pathogen-driven selection in the rainforest. Finally, we find that genes involved in heart and bone development and immune responses are enriched in both selection signals and local hunter-gatherer ancestry in admixed populations, suggesting that selection has maintained adaptive variation in the face of recent gene flow from farmers.

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Lopez M, Choin J, Sikora M, Siddle K, Harmant C, Costa HA et al. Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest. Current Biology. 2019 Sep 9;29(17):2926-2935.e4. https://doi.org/10.1016/j.cub.2019.07.013