Abstract
The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.
| Original language | English |
|---|---|
| Pages (from-to) | 906-913 |
| Number of pages | 8 |
| Journal | Science |
| Volume | 380 |
| Issue number | 6648 |
| Early online date | 1 Jun 2023 |
| DOIs | |
| Publication status | Published - 2 Jun 2023 |
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- 10.1101/2023.05.02.538995Licence: All Rights Reserved
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In: Science, Vol. 380, No. 6648, 02.06.2023, p. 906-913.
Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - A global catalog of whole-genome diversity from 233 primate species
AU - Kuderna, Lukas F. K.
AU - Gao, Hong
AU - Janiak, Mareike C.
AU - Kuhlwilm, Martin
AU - Orkin, Joseph D.
AU - Bataillon, Thomas
AU - Manu, Shivakumara
AU - Valenzuela, Alejandro
AU - Bergman, Juraj
AU - Rousselle, Marjolaine
AU - Silva, Felipe Ennes
AU - Agueda, Lidia
AU - Blanc, Julie
AU - Gut, Marta
AU - Vries, Dorien de
AU - Goodhead, Ian
AU - Harris, R. Alan
AU - Raveendran, Muthuswamy
AU - Jensen, Axel
AU - Chuma, Idrissa S.
AU - Horvath, Julie E.
AU - Hvilsom, Christina
AU - Juan, David
AU - Frandsen, Peter
AU - Schraiber, Joshua G.
AU - Melo, Fabiano R. de
AU - Bertuol, Fabrício
AU - Byrne, Hazel
AU - Sampaio, Iracilda
AU - Farias, Izeni
AU - Valsecchi, João
AU - Messias, Malu
AU - Silva, Maria N. F. da
AU - Trivedi, Mihir
AU - Rossi, Rogerio
AU - Hrbek, Tomas
AU - Andriaholinirina, Nicole
AU - Rabarivola, Clément J.
AU - Zaramody, Alphonse
AU - Jolly, Clifford J.
AU - Phillips-Conroy, Jane
AU - Wilkerson, Gregory
AU - Abee, Christian
AU - Simmons, Joe H.
AU - Fernandez-Duque, Eduardo
AU - Kanthaswamy, Sree
AU - Shiferaw, Fekadu
AU - Wu, Dongdong
AU - Zhou, Long
AU - Shao, Yong
AU - Zhang, Guojie
AU - Keyyu, Julius D.
AU - Knauf, Sascha
AU - Le, Minh D.
AU - Lizano, Esther
AU - Merker, Stefan
AU - Navarro, Arcadi
AU - Nadler, Tilo
AU - Khor, Chiea Chuen
AU - Lee, Jessica
AU - Tan, Patrick
AU - Lim, Weng Khong
AU - Kitchener, Andrew C.
AU - Zinner, Dietmar
AU - Gut, Ivo
AU - Melin, Amanda D.
AU - Guschanski, Katerina
AU - Schierup, Mikkel Heide
AU - Beck, Robin M. D.
AU - Umapathy, Govindhaswamy
AU - Roos, Christian
AU - Boubli, Jean P.
AU - Rogers, Jeffrey
AU - Farh, Kyle Kai-How
AU - Bonet, Tomas Marques
N1 - Funding Information: The authors thank the Veterinary and Zoology staff at Wildlife Reserves Singapore for help in obtaining the tissue samples, as well as the Lee Kong Chian Natural History Museum for storage and provision of the tissue samples. We thank H. Doddapaneni, D. M. Muzny, and M. C. Gingras for their support of sequencing at the Baylor College of Medicine Human Genome Sequencing Center. We appreciate the support of R. Gibbs, director of HGSC, for this project and thank Baylor College of Medicine for internal funding. We thank P. Karanth (IISc) and H. N. Kumara (SACON) for collecting and providing some of the samples from India. We acknowledge the support provided by the Council of Scientific and Industrial Research (CSIR), India, to G.U. for the sequencing at the Centre for Cellular and Molecular Biology (CCMB), India. Silhouettes in Fig. 3 were obtained from phylopic.org. The silhouette for Propithecus is credited to Terpsichores and has been published under CC BY-SA 3.0. All other silhouettes are under public domain. This is Duke Lemur Center publication #1559. E.F.D. thanks the Ministry of Production and the Environment of Formosa Province in Argentina for the research presented here. Samples from Amazônia, Brazil, were accessed under SisGen no. A8F3D55. Funding: L.F.K.K. was supported by an EMBO STF 8286. M.K. was supported by “la Caixa” Foundation (ID 100010434), fellowship code LCF/BQ/PR19/11700002, and by the Vienna Science and Technology Fund (WWTF) [10.47379/VRG20001]. J.D.O. was supported by”la Caixa” Foundation (ID 100010434) and the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 847648. The fellowship code is LCF/BQ/PI20/11760004. F.E.S. has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 801505. FES also received funds from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Process nos.: 303286/2014-8, 303579/2014-5, 200502/2015-8, 302140/2020-4, 300365/2021-7, 301407/2021-5, 301925/2021-6), International Primatological Society (Conservation grant), The Rufford Foundation (14861-1, 23117-2, 38786-B), the Margot Marsh Biodiversity Foundation (SMA-CCO-G0023, SMACCOG0037), and Primate Conservation Inc. (no. 1713 and no. 1689). Fieldwork for samples collected in the Brazilian Amazon was funded by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/SISBIOTA Program 563348/2010-0), Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM/ SISBIOTA 2317/2011), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES AUX 3261/2013) to IPF. Sampling of nonhuman primates in Tanzania was funded by the German Research Foundation (KN1097/3-1 to S.K. and RO3055/2-1 to C.R.) and by the US National Science Foundation (BNS83-03506 to J.P.-C.). No animals in Tanzania were sampled purposely for this study. Details of the original study on Treponema pallidum infection can be requested from S.K. Sampling of baboons in Zambia was funded by US NSF grant BCS-1029451 to J.P.-C., C.J.J., and J.R. The research reported in this manuscript was also funded by the Vietnamese Ministry of Science and Technology’s Program 562 (grant no. ĐTĐL. CN-64/19) to M.D.L. A.N.C. is supported by PID2021-127792NB-I00 funded by MCIN/AEI/10.13039/501100011033 (FEDER Una manera de hacer Europa)” and by “Unidad de Excelencia María de Maeztu”, funded by the AEI (CEX2018-000792-M) and Departament de Recerca i Universitats de la Generalitat de Catalunya (GRC 2021 SGR 0467). A.D.M. was supported by the National Sciences and Engineering Research Council of Canada and Canada Research Chairs program. T.M.B. is supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 864203), PID2021-126004NB-100 (MICIIN/FEDER, UE) and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2021 SGR 00177). M.C.J, D.d.V. I.G., R.M.D.B., and J.P.B. were supported by a UKRI NERC standard grant (NE/T000341/1). S.M.A. was supported by a BINC fellowship from the Department of Biotechnology (DBT), India. Aotus azarae samples from Argentina where obtained with grant support to E.F.-D. from the Zoological Society of San Diego, Wenner-Gren Foundation, the L.S.B. Leakey Foundation, the National Geographic Society, the US National Science Foundation (NSF-BCS-0621020, 1232349, 1503753, 1848954; NSF-RAPID-1219368, NSF-FAIN-1952072; NSF-DDIG-1540255; NSF-REU 0837921, 0924352, 1026991), and the US National Institute on Aging (NIA- P30 AG012836-19, NICHD R24 HD-044964-11). J.H.S. was supported in part by the NIH under award number P40OD024628 - SPF Baboon Research Resource. K.G. was supported by the Swedish Research Council VR (2020-03398). This research is supported by the National Research Foundation Singapore under its National Precision Medicine Programme (NPM) Phase II Funding (MOH-000588) and administered by the Singapore Ministry of Health’s National Medical Research Council. Publisher Copyright: © 2023 American Association for the Advancement of Science. All rights reserved.
PY - 2023/6/2
Y1 - 2023/6/2
N2 - The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.
AB - The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.
U2 - 10.1101/2023.05.02.538995
DO - 10.1101/2023.05.02.538995
M3 - Article
SN - 0036-8075
VL - 380
SP - 906
EP - 913
JO - Science
JF - Science
IS - 6648
ER -