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; Lluis Quintana-Murci

doi:10.1016/j.cub.2019.07.013

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, Lluis Quintana-Murci

10 Citations (Scopus)

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 language	English
Journal	Current Biology
Volume	29
Issue number	17
Pages (from-to)	2926-2935.e4
ISSN	0960-9822
DOIs	https://doi.org/10.1016/j.cub.2019.07.013
Publication status	Published - 9 Sept 2019

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Lopez, M., Choin, J., Sikora, M., Siddle, K., Harmant, C., Costa, H. A., Silvert, M., Mouguiama-Daouda, P., Hombert, J-M., Froment, A., Le Bomin, S., Perry, G. H., Barreiro, L. B., Bustamante, C. D., Verdu, P., Patin, E., & 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, M, Choin, J, Sikora, M, Siddle, K, Harmant, C, Costa, HA, Silvert, M, Mouguiama-Daouda, P, Hombert, J-M, 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

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title = "Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest",

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.",

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

year = "2019",

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doi = "10.1016/j.cub.2019.07.013",

language = "English",

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AU - Lopez, Marie

AU - Choin, Jeremy

AU - Sikora, Martin

AU - Siddle, Katherine

AU - Harmant, Christine

AU - Costa, Helio A.

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, Lluis

PY - 2019/9/9

Y1 - 2019/9/9

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.

AB - 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.

U2 - 10.1016/j.cub.2019.07.013

DO - 10.1016/j.cub.2019.07.013

M3 - Journal article

C2 - 31402299

SN - 0960-9822

VL - 29

SP - 2926-2935.e4

JO - Current Biology

JF - Current Biology

IS - 17

ER -

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

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