Abstract
Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.
| Original language | English (US) |
|---|---|
| Article number | 100133 |
| Journal | Cell Genomics |
| Volume | 2 |
| Issue number | 6 |
| DOIs | |
| State | Published - Jun 8 2022 |
| Externally published | Yes |
Keywords
- chimpanzee
- chimpanzee demography
- conservation genomics
- fecal samples
- geolocalization
- hybridization capture
- non-invasive samples
- population dynamics
- population genetics
ASJC Scopus subject areas
- Genetics
- Biochemistry, Genetics and Molecular Biology (miscellaneous)
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In: Cell Genomics, Vol. 2, No. 6, 100133, 08.06.2022.
Research output: Contribution to journal › Article › peer-review
}
TY - JOUR
T1 - Population dynamics and genetic connectivity in recent chimpanzee history
AU - Fontsere, Claudia
AU - Kuhlwilm, Martin
AU - Morcillo-Suarez, Carlos
AU - Alvarez-Estape, Marina
AU - Lester, Jack D.
AU - Gratton, Paolo
AU - Schmidt, Joshua M.
AU - Dieguez, Paula
AU - Aebischer, Thierry
AU - Álvarez-Varona, Paula
AU - Agbor, Anthony
AU - Angedakin, Samuel
AU - Assumang, Alfred K.
AU - Ayimisin, Emmanuel A.
AU - Bailey, Emma
AU - Barubiyo, Donatienne
AU - Bessone, Mattia
AU - Carretero-Alonso, Andrea
AU - Chancellor, Rebecca
AU - Cohen, Heather
AU - Danquah, Emmanuel
AU - Deschner, Tobias
AU - Dunn, Andrew
AU - Dupain, Jef
AU - Egbe, Villard E.
AU - Feliu, Olga
AU - Goedmakers, Annemarie
AU - Granjon, Anne Céline
AU - Head, Josephine
AU - Hedwig, Daniela
AU - Hermans, Veerle
AU - Hernandez-Aguilar, R. Adriana
AU - Imong, Inaoyom
AU - Jones, Sorrel
AU - Junker, Jessica
AU - Kadam, Parag
AU - Kaiser, Mike
AU - Kambere, Mbangi
AU - Kambale, Magloire V.
AU - Kalan, Ammie K.
AU - Kienast, Ivonne
AU - Kujirakwinja, Deo
AU - Langergraber, Kevin
AU - Lapuente, Juan
AU - Larson, Bradley
AU - Laudisoit, Anne
AU - Lee, Kevin
AU - Llana, Manuel
AU - Llorente, Miquel
AU - Marrocoli, Sergio
AU - Morgan, David
AU - Mulindahabi, Felix
AU - Murai, Mizuki
AU - Neil, Emily
AU - Nicholl, Sonia
AU - Nixon, Stuart
AU - Normand, Emma
AU - Orbell, Chris
AU - Ormsby, Lucy J.
AU - Pacheco, Liliana
AU - Piel, Alex
AU - Riera, Laura
AU - Robbins, Martha M.
AU - Rundus, Aaron
AU - Sanz, Crickette
AU - Sciaky, Lilah
AU - Sommer, Volker
AU - Stewart, Fiona A.
AU - Tagg, Nikki
AU - Tédonzong, Luc Roscelin
AU - Ton, Els
AU - van Schijndel, Joost
AU - Vergnes, Virginie
AU - Wessling, Erin G.
AU - Willie, Jacob
AU - Wittig, Roman M.
AU - Yuh, Yisa G.
AU - Yurkiw, Kyle
AU - Zuberbuehler, Klaus
AU - Hecht, Jochen
AU - Vigilant, Linda
AU - Boesch, Christophe
AU - Andrés, Aida M.
AU - Hughes, David A.
AU - Kühl, Hjalmar S.
AU - Lizano, Esther
AU - Arandjelovic, Mimi
AU - Marques-Bonet, Tomas
N1 - Funding Information: We thank the following government agencies for their support in conducting field research in their countries: Ministère de la Recherche Scientifique et de l'Innovation, Cameroon; Ministère des Forêts et de la Faune, Cameroon; Ministère des Eaux et Forêts, Cote d’Ivoire; Ministère de l’Enseignement Supérieur et de la Recherche Scientifique in Côte d’Ivoire; Institut Congolais pour la Conservation de la Nature, DR-Congo; Ministère de la Recherche Scientifique, DR-Congo; Agence Nationale des Parcs Nationaux, Gabon; Center National de la Recherche Scientifique (CENAREST), Gabon; Société Equatoriale d’Exploitation Forestière (SEEF), Gabon; Department of Wildlife and Range Management, Ghana; Forestry Commission, Ghana; Ministère de l'Agriculture de l'Elevage et des Eaux et Forets, Guinea; Instituto da Biodiversidade e das Áreas Protegidas (IBAP), Guinea-Bissau; Ministro da Agricultura e Desenvolvimento Rural, Guinea-Bissau; Forestry Development Authority, Liberia; Eaux et Forets, Mali; Ministre de l'Environnement et de l'Assainissement et du Developpement Durable du Mali; Conservation Society of Mbe Mountains (CAMM), Nigeria; National Park Service, Nigeria; Ministère de l’Economie Forestière, R-Congo; Ministère de le Recherche Scientifique et Technologique, R-Congo; Ministry of Education, Rwanda; Rwanda Development Board, Rwanda; Direction des Eaux, Forêts, et Chasses, Senegal; Reserve Naturelle Communautaire de Dindefelo, Senegal; Ministry of Agriculture, Forestry, and Food Security, Sierra Leone; National Protected Area Authority, Sierra Leone; Tanzania Commission for Science and Technology, Tanzania; Tanzania Wildlife Research Institute, Tanzania; Makerere University Biological Field Station (MUBFS), Uganda; Uganda National Council for Science and Technology (UNCST), Uganda; Uganda Wildlife Authority, Uganda; National Forestry Authority, Uganda; Agence Congolaise de la Faune et des Aires Protégées; and The Wild Chimpanzee Foundation (WCF). Funding Information: Funding: “la Caixa” Foundation doctoral fellowship program LCF/BQ/DE15/10360006 (to C.F.). FPI (Formación de Personal Investigador) PRE2018-083966 from Ministerio de Ciencia , Universidades e Investigación (to M.A.-E.) and CGL2017-82654-P ( MINECO / FEDER , UE) (to E.L.). “la Caixa” Foundation (ID 100010434 ), fellowship code LCF/BQ/PR19/11700002 (to M.K.). Vienna Science and Technology Fund (WWTF) and the City of Vienna project VRG20-001 (to M.K.). The European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 864203 ) (to T.M.-B.). BFU2017-86471-P ( MINECO / FEDER , UE) (to T.M.-B.). “ Unidad de Excelencia María de Maeztu ”, funded by the AEI ( CEX2018-000792-M ) (to T.M.-B.). Howard Hughes International Early Career (to T.M.-B.). NIH 1R01HG010898-01A1 (to T.M.-B.). Secretaria d’Universitats i Recerca and CERCA Program del Departament d’Economia i Coneixement de la Generalitat de Catalunya ( GRC 2017 SGR 880 ) (to T.M.-B.). UCL’s Wellcome Trust ISSF3 award 204841/Z/16/Z (to A.M.A. and J.M.S.). Generalitat de Catalunya ( 2017 SGR-1040 ) (to M. Llorente). Wellcome Trust Investigator Award 202802/Z/16/Z (to D.A.H.). The Pan African Program: The Cultured Chimpanzee (PanAf) is generously funded by the Max Planck Society , the Max Planck Society Innovation Fund, and the Heinz L. Krekeler Foundation . Funding Information: We would like to thank Marc de Manuel, Juan Antonio Rodriguez, Sojung Han, Christopher Barratt, Richard McElreath, and Lauren White for helpful discussion, and Alan Riedel, Katharina Madl, Veronika Staedele, and Amy Heilman for assistance in the laboratory. We thank Martijn Ter Heegde, Nadege Wangue Njomen, Joshua M. Linder, John Hart, Thurston Cleveland Hicks, Arcel Bamba, Richard Tshombe, Bruno Perodeau, Gita Chelluri, Theophile Desarmeaux, Vianet Mihindou, David Fine, Laura Kehoe, Lucy D'Auvergne, Nuria Maldonado, Luz Calia Miramontes Sequeiros, Theo Freeman, Hilde Vanleeuwe, Jean Claude Dengui, Paul Telfer, Michael Masozera, Nicolas Ntare, Alhaji Malikie Siaka, Henk Eshuis, Jill Pruetz, Geoffrey Muhanguzi, Karsten Dierks, Marcel Ketchan Eyong, Manasseh Eno-Nku, Abel Nzeheke, Yasmin Moebius, Floris Aubert, Matthieu Bonnet, Gregory Brazzola, Chloe Cipoletta, Katherine Corogenes, Charlotte Coupland, Bryan Curran, Emmanuel Dilambaka, Dervla Dowd, Kathryn J. Jeffery, Mohamed Kambi, Vincent Lapeyre, Vera Leinert, Giovanna Maretti, Rumen Martin, Amelia Meier, Protais Niyigabae, Robinson Orume, Jodie Preece, Sebastien Regnaut, Emilien Terrade, and Alexander Tickle for assistance in field site coordination and sample collection. We thank the field assistants and volunteers from the Jane Goodall Institute Spain and Senegal for their help with sample collection in Dindefelo. We thank the team of Rescue & Rehabilitation of the Fundació Mona. We thank Agilent for their collaboration in the project. We thank the following government agencies for their support in conducting field research in their countries: Ministère de la Recherche Scientifique et de l'Innovation, Cameroon; Ministère des Forêts et de la Faune, Cameroon; Ministère des Eaux et Forêts, Cote d'Ivoire; Ministère de l'Enseignement Supérieur et de la Recherche Scientifique in Côte d'Ivoire; Institut Congolais pour la Conservation de la Nature, DR-Congo; Ministère de la Recherche Scientifique, DR-Congo; Agence Nationale des Parcs Nationaux, Gabon; Center National de la Recherche Scientifique (CENAREST), Gabon; Société Equatoriale d'Exploitation Forestière (SEEF), Gabon; Department of Wildlife and Range Management, Ghana; Forestry Commission, Ghana; Ministère de l'Agriculture de l'Elevage et des Eaux et Forets, Guinea; Instituto da Biodiversidade e das Áreas Protegidas (IBAP), Guinea-Bissau; Ministro da Agricultura e Desenvolvimento Rural, Guinea-Bissau; Forestry Development Authority, Liberia; Eaux et Forets, Mali; Ministre de l'Environnement et de l'Assainissement et du Developpement Durable du Mali; Conservation Society of Mbe Mountains (CAMM), Nigeria; National Park Service, Nigeria; Ministère de l'Economie Forestière, R-Congo; Ministère de le Recherche Scientifique et Technologique, R-Congo; Ministry of Education, Rwanda; Rwanda Development Board, Rwanda; Direction des Eaux, Forêts, et Chasses, Senegal; Reserve Naturelle Communautaire de Dindefelo, Senegal; Ministry of Agriculture, Forestry, and Food Security, Sierra Leone; National Protected Area Authority, Sierra Leone; Tanzania Commission for Science and Technology, Tanzania; Tanzania Wildlife Research Institute, Tanzania; Makerere University Biological Field Station (MUBFS), Uganda; Uganda National Council for Science and Technology (UNCST), Uganda; Uganda Wildlife Authority, Uganda; National Forestry Authority, Uganda; Agence Congolaise de la Faune et des Aires Protégées; and The Wild Chimpanzee Foundation (WCF). Funding: “la Caixa” Foundation doctoral fellowship program LCF/BQ/DE15/10360006 (to C.F.). FPI (Formación de Personal Investigador) PRE2018-083966 from Ministerio de Ciencia, Universidades e Investigación (to M.A.-E.) and CGL2017-82654-P (MINECO/FEDER, UE) (to E.L.). “la Caixa” Foundation (ID 100010434), fellowship code LCF/BQ/PR19/11700002 (to M.K.). Vienna Science and Technology Fund (WWTF) and the City of Vienna project VRG20-001 (to M.K.). The European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement no. 864203) (to T.M.-B.). BFU2017-86471-P (MINECO/FEDER, UE) (to T.M.-B.). “Unidad de Excelencia María de Maeztu”, funded by the AEI (CEX2018-000792-M) (to T.M.-B.). Howard Hughes International Early Career (to T.M.-B.). NIH 1R01HG010898-01A1 (to T.M.-B.). Secretaria d'Universitats i Recerca and CERCA Program del Departament d'Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880) (to T.M.-B.). UCL's Wellcome Trust ISSF3 award 204841/Z/16/Z (to A.M.A. and J.M.S.). Generalitat de Catalunya (2017 SGR-1040) (to M. Llorente). Wellcome Trust Investigator Award 202802/Z/16/Z (to D.A.H.). The Pan African Program: The Cultured Chimpanzee (PanAf) is generously funded by the Max Planck Society, the Max Planck Society Innovation Fund, and the Heinz L. Krekeler Foundation. T.M.-B. and M.A. conceived and supervised the study. M.A. C.B. and H.S.K. direct the Pan African Program: The Cultured Chimpanzee. P.D. T.A. P.A.-V. A.A. S.A. A.K.A. E.A.A. E.B. D.B. M.B. A.C.-A. R.C. H.C. E.D. T.D. A.D. J.D. V.E.E. O.F. A.G. A.C.G. J.H. D.H. V.H. R.A.H.A. I.I. SJ. J.J. P.K. M.K. M.V.K. A.K.K. I.K. D.K. K.L. J.L. B.L. A.L. K.L. M. Llana, M. Llorente, S.M. D.M. F.M. M.M. E.N. S. Nicholl, S. Nixon, E.N. C.O. L.J.O. L.P. A.P. L.R. M.M.R. A.R. C.S. L.S. V.S. F.A.S. N.T. L.R.T. E.T. J.v.S. V.V. E.G.W. J.W. R.M.W. Y.G.Y. K.Y. and K.Z. supervised, conducted fieldwork, and collected samples. C.F. M.A.-E. J.D.L. J.H. M.A. and E.L. performed experimental laboratory work. C.F. and M.K. performed the analysis. C.M.-S. P.G. J.M.S. L.V. A.M.A. D.A.H. H.S.H. E.L. M.A. and T.M.-B. provided analytical support. C.F. and M.K. wrote the manuscript with input from all coauthors. The authors declare no competing interests. Publisher Copyright: © 2022 The Authors
PY - 2022/6/8
Y1 - 2022/6/8
N2 - Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.
AB - Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.
KW - chimpanzee
KW - chimpanzee demography
KW - conservation genomics
KW - fecal samples
KW - geolocalization
KW - hybridization capture
KW - non-invasive samples
KW - population dynamics
KW - population genetics
UR - http://www.scopus.com/inward/record.url?scp=85142037075&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85142037075&partnerID=8YFLogxK
U2 - 10.1016/j.xgen.2022.100133
DO - 10.1016/j.xgen.2022.100133
M3 - Article
AN - SCOPUS:85142037075
SN - 2666-979X
VL - 2
JO - Cell Genomics
JF - Cell Genomics
IS - 6
M1 - 100133
ER -