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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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.
Custom scripts are available at: https://github.com/zy041225/primate_sex_chromosome.
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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.).
The authors declare no competing interests.
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Supplementary Notes and Supplementary Figs. 1–28.
Include SD1 ‘Dataset overview’, SD2 ‘Y completeness evaluation’ and SD3 ‘Length of different regions among different species’.
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’.
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’.
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’.
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’.
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