A global catalog of whole-genome diversity from 233 primate species

Author:

Kuderna Lukas F. K.12ORCID,Gao Hong2ORCID,Janiak Mareike C.3ORCID,Kuhlwilm Martin145ORCID,Orkin Joseph D.16ORCID,Bataillon Thomas7ORCID,Manu Shivakumara89ORCID,Valenzuela Alejandro1ORCID,Bergman Juraj710ORCID,Rousselle Marjolaine7ORCID,Silva Felipe Ennes1112ORCID,Agueda Lidia13ORCID,Blanc Julie13ORCID,Gut Marta13ORCID,de Vries Dorien3ORCID,Goodhead Ian3ORCID,Harris R. Alan14ORCID,Raveendran Muthuswamy14ORCID,Jensen Axel15ORCID,Chuma Idrissa S.16ORCID,Horvath Julie E.1718192021ORCID,Hvilsom Christina22ORCID,Juan David1ORCID,Frandsen Peter22ORCID,Schraiber Joshua G.2,de Melo Fabiano R.23ORCID,Bertuol Fabrício24ORCID,Byrne Hazel25ORCID,Sampaio Iracilda26,Farias Izeni24ORCID,Valsecchi João272829ORCID,Messias Malu30ORCID,da Silva Maria N. F.31ORCID,Trivedi Mihir9,Rossi Rogerio32ORCID,Hrbek Tomas2433ORCID,Andriaholinirina Nicole34,Rabarivola Clément J.34,Zaramody Alphonse34,Jolly Clifford J.35,Phillips-Conroy Jane36ORCID,Wilkerson Gregory37ORCID,Abee Christian37,Simmons Joe H.37ORCID,Fernandez-Duque Eduardo38ORCID,Kanthaswamy Sree39,Shiferaw Fekadu40,Wu Dongdong41ORCID,Zhou Long42ORCID,Shao Yong41ORCID,Zhang Guojie4243414445ORCID,Keyyu Julius D.46ORCID,Knauf Sascha47ORCID,Le Minh D.48ORCID,Lizano Esther149ORCID,Merker Stefan50ORCID,Navarro Arcadi1515253ORCID,Nadler Tilo54,Khor Chiea Chuen55,Lee Jessica56ORCID,Tan Patrick555758ORCID,Lim Weng Khong575859ORCID,Kitchener Andrew C.60ORCID,Zinner Dietmar616263ORCID,Gut Ivo13ORCID,Melin Amanda D.646566ORCID,Guschanski Katerina1567ORCID,Schierup Mikkel Heide7ORCID,Beck Robin M. D.3ORCID,Umapathy Govindhaswamy89ORCID,Roos Christian68ORCID,Boubli Jean P.3ORCID,Rogers Jeffrey14ORCID,Farh Kyle Kai-How2ORCID,Marques Bonet Tomas1134951ORCID

Affiliation:

1. IBE, Institute of Evolutionary Biology (UPF-CSIC), Department of Medicine and Life Sciences, Universitat Pompeu Fabra. PRBB, C. Doctor Aiguader N88, 08003 Barcelona, Spain.

2. Illumina Artificial Intelligence Laboratory, Illumina Inc., Foster City, CA 94404, USA.

3. School of Science, Engineering & Environment, University of Salford, Salford M5 4WT, UK.

4. Department of Evolutionary Anthropology, University of Vienna, Djerassiplatz 1, 1030 Vienna, Austria.

5. Human Evolution and Archaeological Sciences (HEAS), University of Vienna, Austria.

6. Département d’anthropologie, Université de Montréal, 3150 Jean-Brillant, Montréal, QC H3T 1N8, Canada.

7. Bioinformatics Research Centre, Aarhus University, Aarhus, Denmark.

8. Academy of Scientific and Innovative Research (AcSIR), Ghaziabad 201002, India.

9. Laboratory for the Conservation of Endangered Species, CSIR-Centre for Cellular and Molecular Biology, Hyderabad 500007, India.

10. Section for Ecoinformatics and Biodiversity, Department of Biology, Aarhus University, Aarhus, Denmark.

11. Research Group on Primate Biology and Conservation, Mamirauá Institute for Sustainable Development, Estrada da Bexiga 2584, CEP 69553-225, Tefé, Amazonas, Brazil.

12. Evolutionary Biology and Ecology (EBE), Département de Biologie des Organismes, Université libre de Bruxelles (ULB), Av. Franklin D. Roosevelt 50, CP 160/12, B-1050 Brussels Belgium.

13. CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri I Reixac 4, 08028 Barcelona, Spain.

14. Human Genome Sequencing Center and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

15. Department of Ecology and Genetics, Animal Ecology, Uppsala University, SE-75236 Uppsala, Sweden.

16. Tanzania National Parks, Arusha, Tanzania.

17. North Carolina Museum of Natural Sciences, Raleigh, NC 27601, USA.

18. Department of Biological and Biomedical Sciences, North Carolina Central University, Durham, NC 27707, USA.

19. Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA.

20. Department of Evolutionary Anthropology, Duke University, Durham, NC 27708, USA.

21. Renaissance Computing Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.

22. Copenhagen Zoo, 2000 Frederiksberg, Denmark.

23. Universidade Federal de Viçosa, Viçosa, Brazil.

24. Universidade Federal do Amazonas, Departamento de Genética, Laboratório de Evolução e Genética Animal (LEGAL), Manaus, Amazonas 69080-900, Brazil.

25. Department of Anthropology, University of Utah, Salt Lake City. UT 84102, USA.

26. Universidade Federal do Para, Bragança, Para, Brazil.

27. Research Group on Terrestrial Vertebrate Ecology, Mamirauá Institute for Sustainable Development, Tefé, Amazonas, Brazil.

28. Rede de Pesquisa para Estudos sobre Diversidade, Conservação e Uso da Fauna na Amazônia – RedeFauna, Manaus, Amazonas, Brazil

29. Comunidad de Manejo de Fauna Silvestre en la Amazonía y en Latinoamérica – ComFauna, Iquitos, Loreto, Peru.

30. Universidade Federal de Rondônia, Porto Velho, Rondônia, Brazil.

31. Instituto Nacional de Pesquisas da Amazônia, Manaus, AM, Brazil.

32. Instituto de Biociências, Universidade Federal do Mato Grosso, Cuiabá, MT, Brazil.

33. Department of Biology, Trinity University, San Antonio, TX 78212, USA.

34. Life Sciences and Environment, Technology and Environment of Mahajanga, University of Mahajanga, Mahajanga, Madagascar.

35. Department of Anthropology, New York University, New York, NY 10003, USA.

36. Department of Neuroscience, Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA.

37. Keeling Center for Comparative Medicine and Research, MD Anderson Cancer Center, Bastrop TX 78602, USA.

38. Department of Anthropology, Yale University, New Haven, CT 06511, USA.

39. School of Mathematical and Natural Sciences, Arizona State University, Phoenix, AZ 85004, USA.

40. Guinea Worm Eradication Program, The Carter Center Ethiopia, Addis Ababa, Ethiopia.

41. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China.

42. Center for Evolutionary and Organismal Biology, Zhejiang University School of Medicine, Hangzhou 310058, China.

43. Villum Centre for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark.

44. Liangzhu Laboratory, Zhejiang University Medical Center, 1369 West Wenyi Road, Hangzhou 311121, China.

45. Women’s Hospital, School of Medicine, Zhejiang University, 1 Xueshi Road, Shangcheng District, Hangzhou 310006, China.

46. Tanzania Wildlife Research Institute (TAWIRI), Head Office, P.O. Box 661, Arusha, Tanzania.

47. Institute of International Animal Health/One Health, Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, 17493 Greifswald–Insel Riems, Germany.

48. Department of Environmental Ecology, Faculty of Environmental Sciences, University of Science and Central Institute for Natural Resources and Environmental Studies, Vietnam National University, Hanoi, Vietnam.

49. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain.

50. Department of Zoology, State Museum of Natural History Stuttgart, Stuttgart, Germany.

51. Institució Catalana de Recerca i Estudis Avançats (ICREA) and Universitat Pompeu Fabra. Pg. Luís Companys 23, 08010 Barcelona, Spain.

52. Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Av. Doctor Aiguader, N88, 08003 Barcelona, Spain.

53. BarcelonaBeta Brain Research Center, Pasqual Maragall Foundation, C. Wellington 30, 08005 Barcelona, Spain.

54. Cuc Phuong Commune, Nho Quan District, Ninh Binh Province, Vietnam.

55. Genome Institute of Singapore, Agency for Science, Technology and Research, Singapore.

56. Mandai Nature, 80 Mandai Lake Road, Singapore.

57. SingHealth Duke-NUS Institute of Precision Medicine (PRISM), Singapore.

58. Cancer and Stem Cell Biology Program, Duke-NUS Medical School, Singapore

59. SingHealth Duke-NUS Genomic Medicine Centre, Singapore.

60. Department of Natural Sciences, National Museums Scotland, Chambers Street, Edinburgh EH1 1JF, UK, and School of Geosciences, Drummond Street, Edinburgh EH8 9XP, UK.

61. Cognitive Ethology Laboratory, Germany Primate Center, Leibniz Institute for Primate Research, 37077 Göttingen, Germany.

62. Department of Primate Cognition, Georg-August-Universität Göttingen, 37077 Göttingen, Germany.

63. Leibniz ScienceCampus Primate Cognition, 37077 Göttingen, Germany.

64. Department of Anthropology and Archaeology, University of Calgary, 2500 University Dr NW, Calgary, AB T2N 1N4, Canada.

65. Department of Medical Genetics, University of Calgary, 3330 Hospital Drive NW, HMRB 202, Calgary, AB T2N 4N1, Canada.

66. Alberta Children’s Hospital Research Institute, University of Calgary, 3330 Hospital Drive NW, HMRB 202, Calgary, AB T2N 4N1, Canada.

67. Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh, UK.

68. Gene Bank of Primates and Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

Reference189 articles.

1. A. B. Rylands R. A. Mittermeier “Primate names: Working Taxonomic List of Primates of the IUCN SSC Primate Specialist Group” in Primate Behavioral Ecology 6th edition K. B. Strier Ed. (Routledge New York 2021) pp. 407–428.

2. Branching out: what omics can tell us about primate evolution

3. The Diversity of Primates: From Biomedicine to Conservation Genomics

4. Initial sequence of the chimpanzee genome and comparison with the human genome

5. Comparative and demographic analysis of orang-utan genomes

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