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Genomic Evidence for the Complex Evolutionary History of Macaques (Genus Macaca)

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Abstract

The genus Macaca is widely distributed, occupies a variety of habitats, shows diverse phenotypic characteristics, and is one of the best-studied genera of nonhuman primates. Here, we reported five re-sequencing Macaca genomes, including one M. cyclopis, one M. fuscata, one M. thibetana, one M. silenus, and one M. sylvanus. Together with published genomes of other macaque species, we combined 20 genome sequences of 10 macaque species to investigate the gene introgression and genetic differences among the species. The network analysis of the SNV-fragment trees indicates a reticular phylogeny of macaque species. Combining the results from various analytical methods, we identified extensive ancient introgression events among macaque species. The multiple introgression signals between different species groups were also observed, such as between fascicularis group species and silenus group species. However, gene flow signals between fascicularis and sinica group were not as strong as those between fascicularis group and silenus group. On the other hand, the unidirect gene flow in M. arctoides probably occurred between the progenitor of M. arctoides and the common ancestor of fascicularis group. Our study also shows that the genetic backgrounds and genetic diversity of different macaques vary dramatically among species, even among populations of the same species. In conclusion, using whole genome sequences and multiple methods, we have studied the evolutionary history of the genus Macaca and provided evidence for extensive introgression among the species.

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Data Availability

The raw sequencing reads for de novo sequencing have been submitted to NCBI Short Read Archive under accession number PRJNA779036. The re-sequencing data have been deposited in the NCBI Short Read Archive (SRR11921216-SRR11921219, SRR11927939-SRR11927943, SRR11927944-SRR11927948).

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant numbers 31770415 and 32171607) and US National Science Foundation (NSF1564659). Computing resources for IMa3 analyses were supported by the National Institutes of Health (grant number S10OD020095), National Science Foundation (grant number 1625061), and US Army Research Laboratory contract (W911NF-16-2-0189). We would like to thank Dr. Zhanlong He from the Chinese Academy of Medical Sciences (Kunming), Mrs Song Wang from Nanning Zoo, and professor Don J. Melnick from Columbia University for their kindly providing macaque samples.

Funding

Funding was provided by National Natural Science Foundation of China (Grant Nos. 32171607, 32371696), National Science Foundation (Grant Nos. NSF1564659, 1625061), Foundation for the National Institutes of Health (Grant No. S10OD020095), Army Research Laboratory (Grant No. W911NF-16-2-0189).

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  1. Zhenxin Fan and Rusong Zhang have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, 610065, Sichuan, People’s Republic of China

    Zhenxin Fan, Rusong Zhang, Yang Song, Bisong Yue & Jing Li

  2. Department of Genetics, Rutgers, the State University of New Jersey, Piscataway, NJ, 08854, USA

    Anbo Zhou & Jinchuan Xing

  3. Department of Biology, Center for Computational Genetics and Genomics, Temple University, Philadelphia, PA, USA

    Jody Hey

  4. Graduate School of Information Science and Technology, Hokkaido University, Sapporo, Hokkaido, 060-0814, Japan

    Naoki Osada

  5. National Primate Research Center of Thailand, Chulalongkorn University, Bangkok, Thailand

    Yuzuru Hamada

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Contributions

ZF, BY, and JL contributed to the design of this research. NO, and YH collected the samples. ZF, RZ, YS, AZ, JH, JW, ML, and JX contributed to data analysis. ZF, RZ, YS, AZ, JH, JW, JX, and JL wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Jing Li.

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Fan, Z., Zhang, R., Zhou, A. et al. Genomic Evidence for the Complex Evolutionary History of Macaques (Genus Macaca). J Mol Evol (2024). https://doi.org/10.1007/s00239-024-10166-z

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