Population dynamics and genetic connectivity in recent chimpanzee history

Claudia Fontsere; Martin Kuhlwilm; Carlos Morcillo-Suarez; Marina Alvarez-Estape; Jack D. Lester; Paolo Gratton; Joshua M. Schmidt; Paula Dieguez; Thierry Aebischer; Paula Álvarez-Varona; Anthony Agbor; Samuel Angedakin; Alfred K. Assumang; Emmanuel A. Ayimisin; Emma Bailey; Donatienne Barubiyo; Mattia Bessone; Andrea Carretero-Alonso; Rebecca Chancellor; Heather Cohen; Emmanuel Danquah; Tobias Deschner; Andrew Dunn; Jef Dupain; Villard E. Egbe; Olga Feliu; Annemarie Goedmakers; Anne-Céline Granjon; Josephine Head; Daniela Hedwig; Veerle Hermans; R. Adriana Hernandez-Aguilar; Inaoyom Imong; Sorrel Jones; Jessica Junker; Parag Kadam; Mike Kaiser; Mbangi Kambere; Magloire V. Kambale; Ammie K. Kalan; Ivonne Kienast; Deo Kujirakwinja; Kevin Langergraber; Juan Lapuente; Bradley Larson; Anne Laudisoit; Kevin Lee; Manuel Llana; Miquel Llorente; Sergio Marrocoli; David Morgan; Felix Mulindahabi; Mizuki Murai; Emily Neil; Sonia Nicholl; Stuart Nixon; Emma Normand; Chris Orbell; Lucy J. Ormsby; Liliana Pacheco; Alex Piel; Laura Riera; Martha M. Robbins; Aaron Rundus; Crickette Sanz; Lilah Sciaky; Volker Sommer; Fiona A. Stewart; Nikki Tagg; Luc Roscelin Tédonzong; Els Ton; Joost van Schijndel; Virginie Vergnes; Erin G. Wessling; Jacob Willie; Roman M. Wittig; Yisa G. Yuh; Kyle Yurkiw; Klaus Zuberbuehler; Jochen Hecht; Linda Vigilant; Christophe Boesch; Aida M. Andrés; David A. Hughes; Hjalmar S. Kühl; Esther Lizano; Mimi Arandjelovic; Tomas Marques-Bonet

doi:10.1016/j.xgen.2022.100133

Population dynamics and genetic connectivity in recent chimpanzee history

Claudia Fontsere^*, Martin Kuhlwilm, Carlos Morcillo-Suarez, Marina Alvarez-Estape, Jack D. Lester, Paolo Gratton, Joshua M. Schmidt, Paula Dieguez, Thierry Aebischer, Paula Álvarez-Varona, Anthony Agbor, Samuel Angedakin, Alfred K. Assumang, Emmanuel A. Ayimisin, Emma Bailey, Donatienne Barubiyo, Mattia Bessone, Andrea Carretero-Alonso, Rebecca Chancellor, Heather CohenEmmanuel Danquah, Tobias Deschner, Andrew Dunn, Jef Dupain, Villard E. Egbe, Olga Feliu, Annemarie Goedmakers, Anne-Céline Granjon, Josephine Head, Daniela Hedwig, Veerle Hermans, R. Adriana Hernandez-Aguilar, Inaoyom Imong, Sorrel Jones, Jessica Junker, Parag Kadam, Mike Kaiser, Mbangi Kambere, Magloire V. Kambale, Ammie K. Kalan, Ivonne Kienast, Deo Kujirakwinja, Kevin Langergraber, Juan Lapuente, Bradley Larson, Anne Laudisoit, Kevin Lee, Manuel Llana, Miquel Llorente, Sergio Marrocoli, David Morgan, Felix Mulindahabi, Mizuki Murai, Emily Neil, Sonia Nicholl, Stuart Nixon, Emma Normand, Chris Orbell, Lucy J. Ormsby, Liliana Pacheco, Alex Piel, Laura Riera, Martha M. Robbins, Aaron Rundus, Crickette Sanz, Lilah Sciaky, Volker Sommer, Fiona A. Stewart, Nikki Tagg, Luc Roscelin Tédonzong, Els Ton, Joost van Schijndel, Virginie Vergnes, Erin G. Wessling, Jacob Willie, Roman M. Wittig, Yisa G. Yuh, Kyle Yurkiw, Klaus Zuberbuehler, Jochen Hecht, Linda Vigilant, Christophe Boesch, Aida M. Andrés, David A. Hughes, Hjalmar S. Kühl, Esther Lizano, Mimi Arandjelovic^*, Tomas Marques-Bonet^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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
Article number	100133
Number of pages	39
Journal	Cell Genomics
Volume	2
Issue number	6
DOIs	https://doi.org/10.1016/j.xgen.2022.100133
Publication status	Published - 8 Jun 2022

Keywords

Chimpanzee
Non-invasive samples
Fecal samples
Hybridization capture
Population genetics
Conservation genomics
Geolocalization
Population dynamics
Chimpanzee demography

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Copyright © 2022 The Authors. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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Fontsere, C., Kuhlwilm, M., Morcillo-Suarez, C., Alvarez-Estape, M., Lester, J. D., Gratton, P., Schmidt, J. M., Dieguez, P., Aebischer, T., Álvarez-Varona, P., Agbor, A., Angedakin, S., Assumang, A. K., Ayimisin, E. A., Bailey, E., Barubiyo, D., Bessone, M., Carretero-Alonso, A., Chancellor, R., ... Marques-Bonet, T. (2022). Population dynamics and genetic connectivity in recent chimpanzee history. Cell Genomics, 2(6), Article 100133. https://doi.org/10.1016/j.xgen.2022.100133

@article{2f71841140a5460d837f9b3c571c6617,

title = "Population dynamics and genetic connectivity in recent chimpanzee history",

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.",

keywords = "Chimpanzee, Non-invasive samples, Fecal samples, Hybridization capture, Population genetics, Conservation genomics, Geolocalization, Population dynamics, Chimpanzee demography",

author = "Claudia Fontsere and Martin Kuhlwilm and Carlos Morcillo-Suarez and Marina Alvarez-Estape and Lester, \{Jack D.\} and Paolo Gratton and Schmidt, \{Joshua M.\} and Paula Dieguez and Thierry Aebischer and Paula {\'A}lvarez-Varona and Anthony Agbor and Samuel Angedakin and Assumang, \{Alfred K.\} and Ayimisin, \{Emmanuel A.\} and Emma Bailey and Donatienne Barubiyo and Mattia Bessone and Andrea Carretero-Alonso and Rebecca Chancellor and Heather Cohen and Emmanuel Danquah and Tobias Deschner and Andrew Dunn and Jef Dupain and Egbe, \{Villard E.\} and Olga Feliu and Annemarie Goedmakers and Anne-C{\'e}line Granjon and Josephine Head and Daniela Hedwig and Veerle Hermans and Hernandez-Aguilar, \{R. Adriana\} and Inaoyom Imong and Sorrel Jones and Jessica Junker and Parag Kadam and Mike Kaiser and Mbangi Kambere and Kambale, \{Magloire V.\} and Kalan, \{Ammie K.\} and Ivonne Kienast and Deo Kujirakwinja and Kevin Langergraber and Juan Lapuente and Bradley Larson and Anne Laudisoit and Kevin Lee and Manuel Llana and Miquel Llorente and Sergio Marrocoli and David Morgan and Felix Mulindahabi and Mizuki Murai and Emily Neil and Sonia Nicholl and Stuart Nixon and Emma Normand and Chris Orbell and Ormsby, \{Lucy J.\} and Liliana Pacheco and Alex Piel and Laura Riera and Robbins, \{Martha M.\} and Aaron Rundus and Crickette Sanz and Lilah Sciaky and Volker Sommer and Stewart, \{Fiona A.\} and Nikki Tagg and T{\'e}donzong, \{Luc Roscelin\} and Els Ton and \{van Schijndel\}, Joost and Virginie Vergnes and Wessling, \{Erin G.\} and Jacob Willie and Wittig, \{Roman M.\} and Yuh, \{Yisa G.\} and Kyle Yurkiw and Klaus Zuberbuehler and Jochen Hecht and Linda Vigilant and Christophe Boesch and Andr{\'e}s, \{Aida M.\} and Hughes, \{David A.\} and K{\"u}hl, \{Hjalmar S.\} and Esther Lizano and Mimi Arandjelovic and Tomas Marques-Bonet",

note = "Funding: The European Research Council (ERC) under the European Union{\textquoteright}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 Mar{\'i}a 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{\textquoteright}Universitats i Recerca and CERCA Program del Departament d{\textquoteright}Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880) (to T.M.-B.). UCL{\textquoteright}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.",

year = "2022",

month = jun,

day = "8",

doi = "10.1016/j.xgen.2022.100133",

language = "English",

volume = "2",

journal = "Cell Genomics",

issn = "2666-979X",

publisher = "Cell Press",

number = "6",

}

Fontsere, C, Kuhlwilm, M, Morcillo-Suarez, C, Alvarez-Estape, M, Lester, JD, Gratton, P, Schmidt, JM, Dieguez, P, Aebischer, T, Álvarez-Varona, P, Agbor, A, Angedakin, S, Assumang, AK, Ayimisin, EA, Bailey, E, Barubiyo, D, Bessone, M, Carretero-Alonso, A, Chancellor, R, Cohen, H, Danquah, E, Deschner, T, Dunn, A, Dupain, J, Egbe, VE, Feliu, O, Goedmakers, A, Granjon, A-C, Head, J, Hedwig, D, Hermans, V, Hernandez-Aguilar, RA, Imong, I, Jones, S, Junker, J, Kadam, P, Kaiser, M, Kambere, M, Kambale, MV, Kalan, AK, Kienast, I, Kujirakwinja, D, Langergraber, K, Lapuente, J, Larson, B, Laudisoit, A, Lee, K, Llana, M, Llorente, M, Marrocoli, S, Morgan, D, Mulindahabi, F, Murai, M, Neil, E, Nicholl, S, Nixon, S, Normand, E, Orbell, C, Ormsby, LJ, Pacheco, L, Piel, A, Riera, L, Robbins, MM, Rundus, A, Sanz, C, Sciaky, L, Sommer, V, Stewart, FA, Tagg, N, Tédonzong, LR, Ton, E, van Schijndel, J, Vergnes, V, Wessling, EG, Willie, J, Wittig, RM, Yuh, YG, Yurkiw, K, Zuberbuehler, K, Hecht, J, Vigilant, L, Boesch, C, Andrés, AM, Hughes, DA, Kühl, HS, Lizano, E, Arandjelovic, M & Marques-Bonet, T 2022, 'Population dynamics and genetic connectivity in recent chimpanzee history', Cell Genomics, vol. 2, no. 6, 100133. https://doi.org/10.1016/j.xgen.2022.100133

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: 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.

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 - Non-invasive samples

KW - Fecal samples

KW - Hybridization capture

KW - Population genetics

KW - Conservation genomics

KW - Geolocalization

KW - Population dynamics

KW - Chimpanzee demography

UR - https://www.scopus.com/pages/publications/85142037075

U2 - 10.1016/j.xgen.2022.100133

DO - 10.1016/j.xgen.2022.100133

M3 - Article

SN - 2666-979X

VL - 2

JO - Cell Genomics

JF - Cell Genomics

IS - 6

M1 - 100133

ER -

Population dynamics and genetic connectivity in recent chimpanzee history

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