TY - JOUR
T1 - Genomic Evidence for Local Adaptation of Hunter-Gatherers to the African Rainforest
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, Lluís
N1 - Funding Information:
We thank all the participants for providing the DNA samples used in this study. We also thank Guillaume Laval and Maxime Rotival for useful discussions, Muh-Ching Yee for laboratory assistance, and the “Paléogénomique et Génétique Moléculaire” Platform from the MnHn at the Musée de l'Homme for assistance in sample preparation. This work was supported by the Institut Pasteur , the Centre National de la Recherche Scientifique , the “Histoire du Génome des Populations Humaines Gabonaises” project ( Institut Pasteur /Republic of Gabon), and an Agence Nationale de la Recherche grant “AGRHUM” ( ANR-14-CE02-0003-01 ) to L.Q.-M. M.L. was supported by the Fondation pour la Recherche Médicale ( FDT20170436932 ), and J.C. by the INCEPTION program and the “Ecole Doctorale FIRE - Programme Bettencourt.”
Funding Information:
We thank all the participants for providing the DNA samples used in this study. We also thank Guillaume Laval and Maxime Rotival for useful discussions, Muh-Ching Yee for laboratory assistance, and the ?Pal?og?nomique et G?n?tique Mol?culaire? Platform from the MnHn at the Mus?e de l'Homme for assistance in sample preparation. This work was supported by the Institut Pasteur, the Centre National de la Recherche Scientifique, the ?Histoire du G?nome des Populations Humaines Gabonaises? project (Institut Pasteur/Republic of Gabon), and an Agence Nationale de la Recherche grant ?AGRHUM? (ANR-14-CE02-0003-01) to L.Q.-M. M.L. was supported by the Fondation pour la Recherche M?dicale (FDT20170436932), and J.C. by the INCEPTION program and the ?Ecole Doctorale FIRE - Programme Bettencourt.?, E.P. and L.Q.-M. conceived and supervised the study. M.L. conducted all the analyses and analyzed the data, with contributions from J.C. M. Silvert, and E.P. C.H. performed laboratory work. M. Sikora, K.S. H.C. and C.D.B. generated and/or analyzed whole-genome data. P.M.-D. J.-M.H. A.F. S.L.B. G.H.P. L.B.B. and P.V. assembled the samples. M.L. E.P. and L.Q.-M. wrote the manuscript, with contributions from all authors. The authors declare no competing interests.
Publisher Copyright:
© 2019 Elsevier Ltd
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.
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U2 - 10.1016/j.cub.2019.07.013
DO - 10.1016/j.cub.2019.07.013
M3 - Article
C2 - 31402299
AN - SCOPUS:85071683660
SN - 0960-9822
VL - 29
SP - 2926-2935.e4
JO - Current Biology
JF - Current Biology
IS - 17
ER -