Comparative genomics reveals the hybrid origin of a macaque group

Bao Lin Zhang; Wu Chen; Zefu Wang; Wei Pang; Meng Ting Luo; Sheng Wang; Yong Shao; Wen Qiang He; Yuan Deng; Long Zhou; Jiawei Chen; Min Min Yang; Yajiang Wu; Lu Wang; Hugo Fernández-Bellon; Sandra Molloy; Hélène Meunier; Fanélie Wanert; Lukas Kuderna; Tomas Marques-Bonet; Christian Roos; Xiao Guang Qi; Ming Li; Zhijin Liu; Mikkel Heide Schierup; David N. Cooper; Jianquan Liu; Yong Tang Zheng; Guojie Zhang; Dong Dong Wu

doi:10.1126/sciadv.add3580

Comparative genomics reveals the hybrid origin of a macaque group

Bao Lin Zhang, Wu Chen, Zefu Wang, Wei Pang, Meng Ting Luo, Sheng Wang, Yong Shao, Wen Qiang He, Yuan Deng, Long Zhou, Jiawei Chen, Min Min Yang, Yajiang Wu, Lu Wang, Hugo Fernández-Bellon, Sandra Molloy, Hélène Meunier, Fanélie Wanert, Lukas Kuderna, Tomas Marques-BonetChristian Roos, Xiao Guang Qi, Ming Li, Zhijin Liu, Mikkel Heide Schierup, David N. Cooper, Jianquan Liu, Yong Tang Zheng, Guojie Zhang, Dong Dong Wu

Department of Molecular Biology and Genetics - Bioinformatics Research Centre (BiRC)

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

17 Citations (Scopus)

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.

Original language	English
Article number	eadd3580
Journal	Science Advances
Volume	9
Issue	22
ISSN	2375-2548
DOIs	https://doi.org/10.1126/sciadv.add3580
Publication status	Published - Jun 2023

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Zhang, B. L., Chen, W., Wang, Z., Pang, W., Luo, M. T., Wang, S., Shao, Y., He, W. Q., Deng, Y., Zhou, L., Chen, J., Yang, M. M., Wu, Y., Wang, L., Fernández-Bellon, H., Molloy, S., Meunier, H., Wanert, F., Kuderna, L., ... Wu, D. D. (2023). Comparative genomics reveals the hybrid origin of a macaque group. Science Advances, 9(22), Article eadd3580. https://doi.org/10.1126/sciadv.add3580

@article{943efe9278824fb4af4d9951dd742b68,

title = "Comparative genomics reveals the hybrid origin of a macaque group",

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.",

author = "Zhang, {Bao Lin} and Wu Chen and Zefu Wang and Wei Pang and Luo, {Meng Ting} and Sheng Wang and Yong Shao and He, {Wen Qiang} and Yuan Deng and Long Zhou and Jiawei Chen and Yang, {Min Min} and Yajiang Wu and Lu Wang and Hugo Fern{\'a}ndez-Bellon and Sandra Molloy and H{\'e}l{\`e}ne Meunier and Fan{\'e}lie Wanert and Lukas Kuderna and Tomas Marques-Bonet and Christian Roos and Qi, {Xiao Guang} and Ming Li and Zhijin Liu and Schierup, {Mikkel Heide} and Cooper, {David N.} and Jianquan Liu and Zheng, {Yong Tang} and Guojie Zhang and Wu, {Dong Dong}",

year = "2023",

month = jun,

doi = "10.1126/sciadv.add3580",

language = "English",

volume = "9",

journal = "Science Advances",

issn = "2375-2548",

publisher = "American Association for the Advancement of Science",

number = "22",

}

Zhang, BL, Chen, W, Wang, Z, Pang, W, Luo, MT, Wang, S, Shao, Y, He, WQ, Deng, Y, Zhou, L, Chen, J, Yang, MM, Wu, Y, Wang, L, Fernández-Bellon, H, Molloy, S, Meunier, H, Wanert, F, Kuderna, L, Marques-Bonet, T, Roos, C, Qi, XG, Li, M, Liu, Z, Schierup, MH, Cooper, DN, Liu, J, Zheng, YT, Zhang, G & Wu, DD 2023, 'Comparative genomics reveals the hybrid origin of a macaque group', Science Advances, vol. 9, no. 22, eadd3580. https://doi.org/10.1126/sciadv.add3580

TY - JOUR

T1 - Comparative genomics reveals the hybrid origin of a macaque group

AU - Zhang, Bao Lin

AU - Chen, Wu

AU - Wang, Zefu

AU - Pang, Wei

AU - Luo, Meng Ting

AU - Wang, Sheng

AU - Shao, Yong

AU - He, Wen Qiang

AU - Deng, Yuan

AU - Zhou, Long

AU - Chen, Jiawei

AU - Yang, Min Min

AU - Wu, Yajiang

AU - Wang, Lu

AU - Fernández-Bellon, Hugo

AU - Molloy, Sandra

AU - Meunier, Hélène

AU - Wanert, Fanélie

AU - Kuderna, Lukas

AU - Marques-Bonet, Tomas

AU - Roos, Christian

AU - Qi, Xiao Guang

AU - Li, Ming

AU - Liu, Zhijin

AU - Schierup, Mikkel Heide

AU - Cooper, David N.

AU - Liu, Jianquan

AU - Zheng, Yong Tang

AU - Zhang, Guojie

AU - Wu, Dong Dong

PY - 2023/6

Y1 - 2023/6

N2 - 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.

AB - 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.

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U2 - 10.1126/sciadv.add3580

DO - 10.1126/sciadv.add3580

M3 - Journal article

C2 - 37262187

AN - SCOPUS:85160969104

SN - 2375-2548

VL - 9

JO - Science Advances

JF - Science Advances

IS - 22

M1 - eadd3580

ER -

Comparative genomics reveals the hybrid origin of a macaque group

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