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Science 29 October 1999:
Vol. 286. no. 5441, pp. 964 - 967
DOI: 10.1126/science.286.5441.964

Reports

Four Evolutionary Strata on the Human X Chromosome

Bruce T. Lahn, * David C. Page dagger

Human sex chromosomes evolved from autosomes. Nineteen ancestral autosomal genes persist as differentiated homologs on the X and Y chromosomes. The ages of individual X-Y gene pairs (measured by nucleotide divergence) and the locations of their X members on the X chromosome were found to be highly correlated. Age decreased in stepwise fashion from the distal long arm to the distal short arm in at least four "evolutionary strata." Human sex chromosome evolution was probably punctuated by at least four events, each suppressing X-Y recombination in one stratum, without disturbing gene order on the X chromosome. The first event, which marked the beginnings of X-Y differentiation, occurred about 240 to 320 million years ago, shortly after divergence of the mammalian and avian lineages.

Howard Hughes Medical Institute, Whitehead Institute, and Department of Biology, Massachusetts Institute of Technology, 9 Cambridge Center, Cambridge, MA 02142, USA.
*   Present address: Department of Human Genetics, University of Chicago, 924 East 57th Street, Chicago, IL 60637, USA.

dagger    To whom correspondence should be addressed. E-mail: dcpage{at}wi.mit.edu


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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