Letter | Published:

Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content

Nature 463, 536–539 (28 January 2010) | Download Citation

Subjects

Abstract

The human Y chromosome began to evolve from an autosome hundreds of millions of years ago, acquiring a sex-determining function and undergoing a series of inversions that suppressed crossing over with the X chromosome1,2. Little is known about the recent evolution of the Y chromosome because only the human Y chromosome has been fully sequenced. Prevailing theories hold that Y chromosomes evolve by gene loss, the pace of which slows over time, eventually leading to a paucity of genes, and stasis3,4. These theories have been buttressed by partial sequence data from newly emergent plant and animal Y chromosomes5,6,7,8, but they have not been tested in older, highly evolved Y chromosomes such as that of humans. Here we finished sequencing of the male-specific region of the Y chromosome (MSY) in our closest living relative, the chimpanzee, achieving levels of accuracy and completion previously reached for the human MSY. By comparing the MSYs of the two species we show that they differ radically in sequence structure and gene content, indicating rapid evolution during the past 6 million years. The chimpanzee MSY contains twice as many massive palindromes as the human MSY, yet it has lost large fractions of the MSY protein-coding genes and gene families present in the last common ancestor. We suggest that the extraordinary divergence of the chimpanzee and human MSYs was driven by four synergistic factors: the prominent role of the MSY in sperm production, ‘genetic hitchhiking’ effects in the absence of meiotic crossing over, frequent ectopic recombination within the MSY, and species differences in mating behaviour. Although genetic decay may be the principal dynamic in the evolution of newly emergent Y chromosomes, wholesale renovation is the paramount theme in the continuing evolution of chimpanzee, human and perhaps other older MSYs.

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Accessions

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

cDNA sequences of chimpanzee ampliconic genes have been deposited in GenBank (http://www.ncbi.nlm.nih.gov) under accession numbers AY958084 (BPY2), AY958081 (CDY), AY958083 (DAZ), AY995201/2 (RBMY), AY958082 (TSPY) and AY995203 (XKRY). Chimpanzee testis cDNA sequences have been deposited in GenBank under accession numbers EX654441–EX654483.

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Acknowledgements

We thank L. Brown, V. Frazzoni, G. Rogers and A. Berger for technical assistance, and L. Brown, M. Carmell, G. Dokshin, M. Gill, J. Mueller, K. Romer and Y. Soh for comments on the manuscript. This work was supported by the National Institutes of Health and the Howard Hughes Medical Institute.

Author Contributions J.F.H., H.S., W.C.W., S. Rozen, R.K.W. and D.C.P. planned the project. J.F.H., H.S. and T.P. performed BAC mapping and RT–PCR analysis. T.A.G., P.J.M., R.S.F. and S.D.M. were responsible for finished BAC sequencing. J.F.H. and H.S. performed comparative sequence analyses. S.K.M.v.D. and S. Repping performed FISH analyses. C.F. and B.J.T. flow-sorted chromosomes. D.P.L. and E.R.M. carried out 454 sequencing. J.F.H. and D.C.P. wrote the paper.

Author information

Affiliations

  1. Howard Hughes Medical Institute, Whitehead Institute, and Department of Biology, Massachusetts Institute of Technology, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA

    • Jennifer F. Hughes
    • , Helen Skaletsky
    • , Tatyana Pyntikova
    • , Steve Rozen
    •  & David C. Page

  2. The Genome Center, Washington University School of Medicine, 4444 Forest Park Boulevard, St Louis, Missouri 63108, USA

    • Tina A. Graves
    • , Patrick J. Minx
    • , Robert S. Fulton
    • , Sean D. McGrath
    • , Devin P. Locke
    • , Elaine R. Mardis
    • , Wesley C. Warren
    •  & Richard K. Wilson

  3. Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Academic Medical Center, Amsterdam 1105 AZ, The Netherlands

    • Saskia K. M. van Daalen
    •  & Sjoerd Repping

  4. Division of Human Biology, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North C3-168, Seattle, Washington 98109, USA

    • Cynthia Friedman
    •  & Barbara J. Trask

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Competing interests

We used an Influx sorter for this study. B.J.T.’s spouse receives royalties for his development of this instrument and is employed by a company, Becton-Dickinson, which now markets this instrument.

Corresponding author

Correspondence to David C. Page.

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  1. 1.

    Supplementary Information

    This file contains Supplementary Notes, Supplementary Figures 1-14 with Legends and Supplementary Tables 1-5. Please note that Supplementary Files 1-3 are available at http://jura.wi.mit.edu/page/papers/Hughes_et_al_2009:- File 1 - Sequence family variants – PCR primers and amplification products; File 2 - Fasta file of chimpanzee MSY sequence assembly; File 3 - Chimpanzee – human MSY sequence alignments.

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DOI

https://doi.org/10.1038/nature08700

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