Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway

Nature Genetics volume 38, pages 158–167 (2006)Cite this article

A Corrigendum to this article was published on 01 March 2006

Abstract

The mammalian Y chromosome has unique characteristics compared with the autosomes or X chromosomes. Here we report the finished sequence of the chimpanzee Y chromosome (PTRY), including 271 kb of the Y-specific pseudoautosomal region 1 and 12.7 Mb of the male-specific region of the Y chromosome. Greater sequence divergence between the human Y chromosome (HSAY) and PTRY (1.78%) than between their respective whole genomes (1.23%) confirmed the accelerated evolutionary rate of the Y chromosome. Each of the 19 PTRY protein-coding genes analyzed had at least one nonsynonymous substitution, and 11 genes had higher nonsynonymous substitution rates than synonymous ones, suggesting relaxation of selective constraint, positive selection or both. We also identified lineage-specific changes, including deletion of a 200-kb fragment from the pericentromeric region of HSAY, expansion of young Alu families in HSAY and accumulation of young L1 elements and long terminal repeat retrotransposons in PTRY. Reconstruction of the common ancestral Y chromosome reflects the dynamic changes in our genomes in the 5–6 million years since speciation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematic view of the sequenced area and major landmarks on chimpanzee chromosome Y.
Figure 2: Features of the PTRY sequence.
Figure 3: Comparison of the PAR1 and MSY regions of PTRY.
Figure 4: Evolutionary relationship between inserted repetitive elements.
Figure 5: Synteny blocks in the sequenced region of PTRY and comparison with HSAY.
Figure 6: Comparison of the palindromic structures between PTRY and HSAY.

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

References

  1. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).

  2. International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature 431, 931–945 (2004).

  3. Gagneux, P. & Varki, A. Genetic differences between humans and great apes. Mol. Phylogenet. Evol. 18, 2–13 (2001).

    Article  CAS  Google Scholar 

  4. Fujiyama, A. et al. Construction and analysis of a human-chimpanzee comparative clone map. Science 295, 131–134 (2002).

    Article  Google Scholar 

  5. Ebersberger, I., Metzler, D., Schwarz, C. & Paabo, S. Genomewide comparison of DNA sequences between humans and chimpanzees. Am. J. Hum. Genet. 70, 1490–1497 (2002).

    Article  CAS  Google Scholar 

  6. Chou, H.H. et al. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc. Natl. Acad. Sci. USA 99, 11736–11741 (2002).

    Article  CAS  Google Scholar 

  7. Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869–872 (2002).

    Article  CAS  Google Scholar 

  8. Sakaki, Y. et al. Human versus chimpanzee chromosome-wide sequence comparison and its evolutionary implication. Cold Spring Harb. Symp. Quant. Biol. 68, 455–460 (2003).

    Article  CAS  Google Scholar 

  9. Olson, M.V. & Varki, A. Sequencing the chimpanzee genome: insights into human evolution and disease. Nat. Rev. Genet. 4, 20–28 (2003).

    Article  CAS  Google Scholar 

  10. The International Chimpanzee Chromosome 22 Consortium. DNA sequence and comparative analysis of chimpanzee chromosome 22. Nature 429, 382–388 (2004).

  11. Ptak, S.E. et al. Fine-scale recombination patterns differ between chimpanzees and humans. Nat. Genet. 37, 429–434 (2005).

    Article  CAS  Google Scholar 

  12. Ohno, S. Sex Chromosomes and Sex-Linked Genes (Springer, Berlin, 1967).

    Book  Google Scholar 

  13. Bishop, C. et al. Extensive sequence homologies between Y and other human chromosomes. J. Mol. Biol. 173, 403–417 (1984).

    Article  CAS  Google Scholar 

  14. Graves, J.A. The origin and function of the mammalian Y chromosome and Y-borne genes–an evolving understanding. Bioessays 17, 311–320 (1995).

    Article  CAS  Google Scholar 

  15. Lahn, B.T. & Page, D.C. Four evolutionary strata on the human X chromosome. Science 286, 964–967 (1999).

    Article  CAS  Google Scholar 

  16. Waters, P.D. et al. The human Y chromosome derives largely from a single autosomal region added to the sex chromosomes 80–130 million years ago. Cytogenet. Cell Genet. 92, 74–76 (2001).

    Article  CAS  Google Scholar 

  17. Lahn, B.T., Pearson, N.M. & Jegalian, K. The human Y chromosome, in the light of evolution. Nat. Rev. Genet. 2, 207–216 (2001).

    Article  CAS  Google Scholar 

  18. Page, D.C., Harper, M.E., Love, J. & Botstein, D. Occurrence of a transposition from the X-chromosome long arm to the Y-chromosome short arm during human evolution. Nature 311, 119–123 (1984).

    Article  CAS  Google Scholar 

  19. Skaletsky, H. et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837 (2003).

    Article  CAS  Google Scholar 

  20. Ross, M.T. et al. The DNA sequence of the human X chromosome. Nature 434, 325–337 (2005).

    Article  CAS  Google Scholar 

  21. Archidiacono, N. et al. Evolution of chromosome Y in primates. Chromosoma 107, 241–246 (1998).

    Article  CAS  Google Scholar 

  22. Gerrard, D.T. & Filatov, D.A. Positive and negative selection on mammalian Y chromosomes. Mol. Biol. Evol. 22, 1423–1432 (2005).

    Article  CAS  Google Scholar 

  23. Miyata, T. et al. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb. Symp. Quant. Biol. 52, 863–867 (1987).

    Article  CAS  Google Scholar 

  24. Erlandsson, R., Wilson, J.F. & Paabo, S. Sex chromosomal transposable element accumulation and male-driven substitutional evolution in humans. Mol. Biol. Evol. 17, 804–812 (2000).

    Article  CAS  Google Scholar 

  25. Makova, K.D. & Li, W.H. Strong male-driven evolution of DNA sequences in humans and apes. Nature 416, 624–626 (2002).

    Article  CAS  Google Scholar 

  26. Saitou, N. & Ueda, S. Evolutionary rate of insertions and deletions in non-coding nucleotide sequences of primates. Mol. Biol. Evol. 11, 504–512 (1994).

    CAS  PubMed  Google Scholar 

  27. Stone, A.C. et al. High levels of Y-chromosome nucleotide diversity in the genus Pan. Proc. Natl. Acad. Sci. USA 99, 43–48 (2002).

    Article  CAS  Google Scholar 

  28. Filatov, D.A. A gradient of silent substitution rate in the human pseudoautosomal region. Mol. Biol. Evol. 21, 410–417 (2004).

    Article  CAS  Google Scholar 

  29. Bailey, J.A. et al. Recent segmental duplications in the human genome. Science 297, 1003–1007 (2002).

    Article  CAS  Google Scholar 

  30. Liu, G. et al. Analysis of primate genomic variation reveals a repeat-driven expansion of the human genome. Genome Res. 13, 358–368 (2003).

    Article  CAS  Google Scholar 

  31. Hedges, D.J. et al. Differential Alu mobilization and polymorphism among the human and chimpanzee lineages. Genome Res. 14, 1068–1075 (2004).

    Article  CAS  Google Scholar 

  32. Orti, R. et al. Conservation of pericentromeric duplications of a 200-kb part of the human 21q22.1 region in primates. Cytogenet. Cell Genet. 83, 262–265 (1998).

    Article  CAS  Google Scholar 

  33. Golfier, G. et al. The 200-kb segmental duplication on human chromosome 21 originates from a pericentromeric dissemination involving human chromosomes 2, 18 and 13. Gene 312, 51–59 (2003).

    Article  CAS  Google Scholar 

  34. Bonner, T.I. et al. Molecular cloning of a family of retroviral sequences found in chimpanzee but not human DNA. J. Virol. 43, 914–924 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Kjellman, C., Sjogren, H.O. & Widegren, B. The Y chromosome: a graveyard for endogenous retroviruses. Gene 161, 163–170 (1995).

    Article  CAS  Google Scholar 

  36. Yohn, C.T. et al. Lineage-specific expansions of retroviral insertions within the genomes of African great apes but not humans and orangutans. PLoS Biol. 3, e110 (2005).

    Article  Google Scholar 

  37. Gibbons, R. et al. Distinguishing humans from great apes with AluYb8 repeats. J. Mol. Biol. 339, 721–729 (2004).

    Article  CAS  Google Scholar 

  38. Han, K. et al. Under the genomic radar: the stealth model of Alu amplification. Genome Res. 15, 655–664 (2005).

    Article  CAS  Google Scholar 

  39. Schwartz, A. et al. Reconstructing hominid Y evolution: X-homologous block, created by X-Y transposition, was disrupted by Yp inversion through LINE-LINE recombination. Hum. Mol. Genet. 7, 1–11 (1998).

    Article  CAS  Google Scholar 

  40. Rosen, S. et al. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423, 873–876 (2003).

    Article  Google Scholar 

  41. Li, W.-H . Molecular Evolution 237–267 (Sinauer, Sunderland, Massachusetts, 1997).

    Google Scholar 

  42. Thomson, R., Pitchard, J.K., Shen, P., Oefner, P.J. & Feldman, M.W. Recent common ancestry of human y chromosomes: Evidence from DNA sequence data. Proc. Natl. Acad. Sci. USA 97, 7360–7365 (2000).

    Article  CAS  Google Scholar 

  43. Underhill, P.A. et al. Detection of numerous Y chromosome biallelic polymorphisms by denaturing high-performance liquid chromatography. Genome Res. 7, 947–949 (1997).

    Article  Google Scholar 

  44. Underhill, P.A. et al. Y chromosome sequence variation and the history of human populations. Nat. Genet. 26, 358–361 (2000).

    Article  CAS  Google Scholar 

  45. The Y Chromosome Consortium. A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res. 12, 339–348 (2002).

  46. Kittler, R. et al. Apparent intrachromosomal exchange on the human Y chromosome explained by population history. Eur. J. Hum. Genet. 11, 304–314 (2003).

    Article  CAS  Google Scholar 

  47. Kuroki, Y. et al. Spermatogenic ability is different among males in different Y chromosome lineage. J. Hum. Genet. 44, 289–292 (1999).

    Article  CAS  Google Scholar 

  48. Nakahori, Y. The Y chromosome-a hypothesis on the evolution of sex chromosomes. in Sexual Differentiation and Maturation. Frontier in Endocrinology 17 (Hibi, I. & Tanaka, T., eds.) 1–14 (Ares-Serono Symposia Publications, Rome, 1996).

    Google Scholar 

  49. Yamada, T. & Morishita, S. Computing highly specific and noise tolerant oligomers efficiently. J. Bioinform. Comput. Biol. 2, 21–46 (2004).

    Article  CAS  Google Scholar 

  50. Brudno, M. et al. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res. 13, 721–731 (2003).

    Article  CAS  Google Scholar 

  51. Hughes, J.F. et al. Conservation of Y-linked genes during human evolution revealed by comparative sequencing. Nature 437, 100–105 (2005).

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to all the technical staff of RIKEN Genomic Sciences Center (RIKEN-GSC) and Genome Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB). In addition, we wish to thank Y. Nakahori (Tokushima University), T. Matsuzawa (Primate Research Institute, Kyoto University), T. Ishida (The University of Tokyo), N. Collier (National Institute of Informatics) for the supply of the human and chimpanzee samples, and discussion. We also thank the Osaka Municipal Tennoji (Osaka, Japan) for discussions on the subspecies of chimpanzee. We would also like to thank A. Frankish, E. Hart and J. Harrow from the HAVANA group, the Wellcome Trust Sanger Institute, for providing annotation of the human Y chromosome. We are also thankful for D.C. Page (Whitehead Institute), R.K. Wilson (Washington University School of Medicine) and the Chimpanzee Sequencing and Analysis Consortium for the availability of the sequences in the public databases. This work was supported in part by: Special Fund for RIKEN-GSC; Grant-in-Aid for Scientific Research on Priority Areas “Genome Science” from the Ministry of Education, Culture, Sports, Science and Technology, Japan; The Ministry of Science & Technology, Korea, and Special Fund of KRIBB, Korea.

Author information

Authors and Affiliations

  1. RIKEN Genomic Sciences Center, Yokohama, 230-0045, Japan

    Yoko Kuroki, Atsushi Toyoda, Hideki Noguchi, Todd D Taylor, Masahira Hattori, Yoshiyuki Sakaki & Asao Fujiyama

  2. Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, 277-0882, Japan

    Hideki Noguchi, Tomoyuki Yamada & Shinichi Morishita

  3. Mitsubishi Research Institute, Tokyo, 100-8141, Japan

    Takehiko Itoh

  4. Genome Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, 305-333, Korea

    Dae-Soo Kim, Dae-Won Kim, Sang-Haeng Choi, Il-Chul Kim, Han Ho Choi, Yong Sung Kim & Hong-Seog Park

  5. University of Science and Technology, Daejeon, 305-333, Korea

    Dae-Won Kim & Hong-Seog Park

  6. The Graduate University for Advanced Studies, Hayama, 240-0193, Japan

    Yoko Satta

  7. National Institute of Genetics, Mishima, 411-8540, Japan

    Naruya Saitou

  8. Kitasato University, Sagamihara, 228-8555, Japan

    Masahira Hattori

  9. National Institute of Informatics, Tokyo, 101-8430, Japan

    Asao Fujiyama

Authors
  1. Yoko Kuroki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Atsushi Toyoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hideki Noguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Todd D Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takehiko Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dae-Soo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dae-Won Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sang-Haeng Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Il-Chul Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Han Ho Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yong Sung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yoko Satta
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Naruya Saitou
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Tomoyuki Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Shinichi Morishita
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Masahira Hattori
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Yoshiyuki Sakaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Hong-Seog Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Asao Fujiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hong-Seog Park or Asao Fujiyama.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Gene landscape of PTRY. (PDF 695 kb)

Supplementary Fig. 2

Presence or absence of CD24L4 in primates. (PDF 148 kb)

Supplementary Fig. 3

Correlation between nucleotide substitution and indel frequencies. (PDF 329 kb)

Supplementary Fig. 4

Analysis of the 200 kb duplicated segments. (PDF 176 kb)

Supplementary Fig. 5

Structural changes of human and chimpanzee Y chromosome during sex chromosome evolution. (PDF 225 kb)

Supplementary Fig. 6

Features of the PTRY ampliconic units. (PDF 94 kb)

Supplementary Table 1

List of the clones analyzed in this study. (PDF 37 kb)

Supplementary Table 2

List of annotated genes. (PDF 93 kb)

Supplementary Table 3

Gene analysis. (PDF 17 kb)

Supplementary Table 4

Summary of base substitutions between PTRY and HSAY, and between PTR22 and HSA21. (PDF 14 kb)

Supplementary Table 5

List of accession numbers for the clones used in this study. (PDF 17 kb)

Supplementary Table 6

Positions of LINE1 and Alu sequences in the HSAY and PTRY sequences. (PDF 21 kb)

Supplementary Table 7

Positions of the synteny blocks and the alignments. (PDF 13 kb)

Supplementary Methods (PDF 23 kb)

Supplementary Note (PDF 36 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuroki, Y., Toyoda, A., Noguchi, H. et al. Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nat Genet 38, 158–167 (2006). https://doi.org/10.1038/ng1729

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1729

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing