Comparative genomics reveals the hybrid origin of a macaque group

Author:

Zhang Bao-Lin1ORCID,Chen Wu2ORCID,Wang Zefu34ORCID,Pang Wei5ORCID,Luo Meng-Ting5,Wang Sheng1ORCID,Shao Yong1ORCID,He Wen-Qiang5,Deng Yuan67ORCID,Zhou Long8ORCID,Chen Jiawei6,Yang Min-Min1,Wu Yajiang2,Wang Lu9,Fernández-Bellon Hugo10ORCID,Molloy Sandra11ORCID,Meunier Hélène1213,Wanert Fanélie14ORCID,Kuderna Lukas15ORCID,Marques-Bonet Tomas16171819ORCID,Roos Christian2021ORCID,Qi Xiao-Guang9ORCID,Li Ming22ORCID,Liu Zhijin23,Schierup Mikkel Heide24ORCID,Cooper David N.25ORCID,Liu Jianquan326ORCID,Zheng Yong-Tang527ORCID,Zhang Guojie182829ORCID,Wu Dong-Dong1273031ORCID

Affiliation:

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

2. Guangzhou Zoo and Guangzhou Wildlife Research Center, Guangzhou 510070, China.

3. Key Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China.

4. Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China.

5. Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences, KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.

6. BGI-Shenzhen, Shenzhen 518083, China.

7. Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen DK-2100, Denmark.

8. Center for Evolutionary and Organismal Biology and Women’s Hospital at Zhejiang University School of Medicine, Hangzhou 310058, China.

9. Shaanxi Key Laboratory for Animal Conservation, College of Life Sciences, Northwest University, Xi’an, China.

10. Barcelona Zoo, Parc de La Ciutadella, Barcelona 08003, Spain.

11. Dublin Zoo, Dublin 8, Ireland.

12. Centre de Primatologie, de l'Université de Strasbourg, Niederhausbergen, France.

13. Laboratoire de Neurosciences Cognitives et Adaptatives, UMR 7364, Université de Strasbourg, Strasbourg, France.

14. Plateforme SILABE, Université de Strasbourg, Niederhausbergen, France.

15. Genome Interpretation Department, Illumina Inc., Foster City, CA, USA.

16. Institute of Evolutionary Biology (UPF-CSIC), PRBB, Dr. Aiguader 88, Barcelona 08003, Spain.

17. Catalan Institution of Research and Advanced Studies (ICREA), Passeig de Lluís Companys, 23, Barcelona 08010, Spain.

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

19. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Edifici ICTA-ICP, c/Columnes s/n, 08193 Cerdanyola del Vallès, Barcelona, Spain.

20. Primate Genetics Laboratory, German Primate Center, Göttingen, Germany.

21. Gene Bank of Primates, German Primate Center, Göttingen, Germany.

22. CAS Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

23. College of Life Sciences, Capital Normal University, Beijing 100048, China.

24. Bioinformatics Research Centre, Aarhus University, Aarhus C DK-8000, Denmark.

25. Institute of Medical Genetics, School of Medicine, Cardiff University, Cardiff CF14 4XN, UK.

26. State Key Laboratory of Grassland Agro-ecosystem, Institute of Innovation Ecology and College of Life Sciences, Lanzhou University, Lanzhou 730000, China.

27. National Resource Center for Non-Human Primates, Kunming Primate Research Center and National Research Facility for Phenotypic and Genetic Analysis of Model Animals (Primate Facility), Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650107, China.

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

29. Villum Center for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen 2100, Denmark.

30. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China.

31. Kunming Natural History Museum of Zoology, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China.

Abstract

Although species can arise through hybridization, compelling evidence for hybrid speciation has been reported only rarely in animals. Here, we present phylogenomic analyses on genomes from 12 macaque species and show that the fascicularis group originated from an ancient hybridization between the sinica and silenus groups ~3.45 to 3.56 million years ago. The X chromosomes and low-recombination regions exhibited equal contributions from each parental lineage, suggesting that they were less affected by subsequent backcrossing and hence could have played an important role in maintaining hybrid integrity. We identified many reproduction-associated genes that could have contributed to the development of the mixed sexual phenotypes characteristic of the fascicularis group. The phylogeny within the silenus group was also resolved, and functional experimentation confirmed that all extant Western silenus species are susceptible to HIV-1 infection. Our study provides novel insights into macaque evolution and reveals a hybrid speciation event that has occurred only very rarely in primates.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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