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Eighty million years of rapid evolution of the primate Y chromosome

Nature Ecology & Evolution volume 7, pages 1114–1130 (2023)Cite this article

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Abstract

The Y chromosome usually plays a critical role in determining male sex and comprises sequence classes that have experienced unique evolutionary trajectories. Here we generated 19 new primate sex chromosome assemblies, analysed them with 10 existing assemblies and report rapid evolution of the Y chromosome across primates. The pseudoautosomal boundary has shifted at least six times during primate evolution, leading to the formation of a Simiiformes-specific evolutionary stratum and to the independent start of young strata in Catarrhini and Platyrrhini. Different primate lineages experienced different rates of gene loss and structural and chromatin change on their Y chromosomes. Selection on several Y-linked genes has contributed to the evolution of male developmental traits across the primates. Additionally, lineage-specific expansions of ampliconic regions have further increased the diversification of the structure and gene composition of the Y chromosome. Overall, our comprehensive analysis has broadened our knowledge of the evolution of the primate Y chromosome.

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Fig. 1: Overview of the X and Y assemblies used in this study.
Fig. 2: The evolution of the primate PAR.
Fig. 3: Evolutionary strata of primates.
Fig. 4: Structural and chromatin configuration changes in S4 and S5 during primate sex chromosome evolution.
Fig. 5: Dynamic evolution of primate Y chromosomes.
Fig. 6: Comparison of X-linked (a) and Y-linked (b) families involving AGs across the primates and treeshrew.

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Data availability

Primate long- and short-read sequencing data were obtained from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) Database (https://www.ncbi.nlm.nih.gov/sra/) under accession code PRJNA785018, PRJNA658635 and PRJEB49549, and the GSA database with project no. PRJCA003786. Sequencing data and curated assemblies used in this study have been deposited in the NCBI Assembly Database (https://www.ncbi.nlm.nih.gov/assembly/) under accession code PRJNA790674 and the CNGB Sequence Archive (CNSA) of China National GeneBank DataBase (CNGBdb) with accession number CNP0002500. Human diploid Hi-C mapping data were obtained from https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE63525. Other data are available in the main text or the supplementary data. Analytical data have been deposited into figshare with the link https://doi.org/10.6084/m9.figshare.20115467.v1.

Code availability

Custom scripts are available at: https://github.com/zy041225/primate_sex_chromosome.

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Acknowledgements

We thank all supervisors, collaborators and anyone else involved with the collection and processing of the primary datasets. We thank China National GeneBank for providing the computational resources. This study was supported by grants from Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31020000 to G.Z.), International Partnership Program of Chinese Academy of Sciences (no. 152453KYSB20170002 to G.Z.), Villum Investigator Grant (no. 25900 to G.Z.), National Natural Science Foundation of China (31822048 to D.-D.W.), Yunnan Fundamental Research Project (2019FI010 to D.-D.W.) and The Animal Branch of the Germplasm Bank of Wild Species of Chinese Academy of Science (the Large Research Infrastructure Funding to D.-D.W.).

Author information

Authors and Affiliations

  1. BGI-Shenzhen, Shenzhen, China

    Yang Zhou, Xiaoyu Zhan, Jiazheng Jin, Xuemei Li, Miaoquan Fang, Jiawei Chen, Qi Fang & Huanming Yang

  2. Centre for Evolutionary & Organismal Biology, and Women’s Hospital, Zhejiang University School of Medicine, Hangzhou, China

    Long Zhou & Guojie Zhang

  3. Liangzhu Laboratory, Zhejiang University Medical Center, Hangzhou, China

    Long Zhou & Guojie Zhang

  4. Section for Ecoinformatics & Biodiversity, Department of Biology, Aarhus University, Aarhus C., Denmark

    Juraj Bergman

  5. Bioinformatics Research Centre, Aarhus University, Aarhus C., Denmark

    Juraj Bergman, Marjolaine Marie C. Rousselle, Meritxell Riera Belles & Mikkel Heide Schierup

  6. College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China

    Xuemei Li & Huanming Yang

  7. College of Life Sciences, Northwest University, Xi’an, China

    Lan Zhao & Xiaoguang Qi

  8. Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain

    Lukas Kuderna & Tomas Marques-Bonet

  9. Catalan Institution of Research and Advanced Studies (ICREA), Barcelona, Spain

    Tomas Marques-Bonet

  10. CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain

    Tomas Marques-Bonet

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

    Tomas Marques-Bonet

  12. Graduate School of Environmental Science, Hokkaido University, Sapporo, Japan

    Haruka Kitayama

  13. Faculty of Environmental Earth Science, Hokkaido University, Sapporo, Japan

    Takashi Hayakawa

  14. Japan Monkey Centre, Inuyama, Japan

    Takashi Hayakawa

  15. Kunming College of Life Science, University of the Chinese Academy of Sciences, Kunming, China

    Yong-Gang Yao

  16. Key Laboratory of Animal Models and Human Disease Mechanisms of Chinese Academy of Sciences & Yunnan Province, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    Yong-Gang Yao

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

    Yong-Gang Yao & Dong-Dong Wu

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

    Yong-Gang Yao & Dong-Dong Wu

  19. KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    Yong-Gang Yao & Dong-Dong Wu

  20. James D. Watson Institute of Genome Sciences, Hangzhou, China

    Huanming Yang

  21. Guangdong Provincial Academician Workstation of BGI Synthetic Genomics, BGI-Shenzhen, Shenzhen, China

    Huanming Yang

  22. The Cancer Hospital of the University of Chinese Academy of Sciences (Zhejiang Cancer Hospital), Institute of Basic Medicine and Cancer (IBMC), Chinese Academy of Sciences, Hangzhou, China

    Huanming Yang

  23. Institute of Medical Genetics, School of Medicine, Cardiff University, Cardiff, UK

    David N. Cooper

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

    Dong-Dong Wu & Guojie Zhang

  25. Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark

    Guojie Zhang

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  1. Yang Zhou
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Contributions

G.Z. conceived the project. D.-D.W., H.K., T.H., Y.-G.Y., La.Z., X.Q., L.K. and T.M.-B. coordinated and were involved in sample collection, extraction and sequencing. Y.Z., X.Z., J.J., Lo.Z., J.B., X.L., M.M.C.R., M.R.B., M.F., J.C. and Q.F. performed the analyses. G.Z., M.H.S. and H.Y. supervised the project. G.Z., D.N.C., M.H.S., Y.Z., M.R.B., J.B., M.M.C.R., Y.-G.Y. and T.M.-B. wrote the manuscript with input from all the authors.

Corresponding author

Correspondence to Guojie Zhang.

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Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Qi Zhou and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Supplementary information

Supplementary Information

Supplementary Notes and Supplementary Figs. 1–28.

Reporting Summary

Peer Review File

Supplementary Data 1–3

Include SD1 ‘Dataset overview’, SD2 ‘Y completeness evaluation’ and SD3 ‘Length of different regions among different species’.

Supplementary Data 4 and 5

Include SD4 ‘Gametologue pairs and pairwise dS in 30 species in this study’ and SD5 ‘Per position per year (PPPY) estimates of the autosomal mutation rate μ for different primates and mouse’.

Supplementary Data 6–9

Include SD6 ‘X/Y homologous blocks within S4, S5 and their SSIM and SN’, SD7 ‘Syntenic blocks between prosimian and other species, and their SSIM and SN’, SD8 ‘Syntenic blocks between treeshrew and other species, and their SSIM and SN’ and SD9 ‘TAD boundary conservation between Simiiformes and treeshrew or pygmy slow loris’.

Supplementary Data 10–13

Include SD10 ‘Y gene family cluster results’, SD11 ‘Y loss dynamics of S4/S5 Y-linked genes’, SD12 ‘Life history traits of the primates used in this study’ and SD13 ‘PGLS results’.

Supplementary Data 14–18

Include SD14 ‘X-linked families involved AGs’, SD15 ‘Y-linked families involved AGs’, SD16 ‘Statistics and Fisher exact test of X-linked gene families that contains AGs’, SD17 ‘AG X/Y co-amplification’ and SD18 ‘Data and species used in each analysis’.

Supplementary Data 19–23

Include SD19 ‘Frameshifts check of potential Y pseudogenes with male short reads’, SD20 ‘Frameshifts check of potential X pseudogenes with male short reads’, SD21 ‘Potential Y absent gene confirmation from raw long reads’, SD22 ‘Potential Y absent gene confirmation from male short reads’ and SD23 ‘Potential X absent gene confirmation from raw long reads’.

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Zhou, Y., Zhan, X., Jin, J. et al. Eighty million years of rapid evolution of the primate Y chromosome. Nat Ecol Evol 7, 1114–1130 (2023). https://doi.org/10.1038/s41559-022-01974-x

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