Woot! Men still evolving! See, not doomed to obsolescence, are we?

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Letter

Nature 463, 536-539 (28 January 2010) | doi:10.1038/nature08700; Received 3 August 2009; Accepted 24 November 2009; Published online 13 January 2010

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

Jennifer F. Hughes¹, Helen Skaletsky¹, Tatyana Pyntikova¹, Tina A. Graves², Saskia K. M. van Daalen³, Patrick J. Minx², Robert S. Fulton², Sean D. McGrath², Devin P. Locke², Cynthia Friedman⁴, Barbara J. Trask⁴, Elaine R. Mardis², Wesley C. Warren², Sjoerd Repping³, Steve Rozen¹, Richard K. Wilson² & David C. Page¹

1. Howard Hughes Medical Institute, Whitehead Institute, and Department of Biology, Massachusetts Institute of Technology, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA
2. The Genome Center, Washington University School of Medicine, 4444 Forest Park Boulevard, St Louis, Missouri 63108, USA
3. Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Academic Medical Center, Amsterdam 1105 AZ, The Netherlands
4. Division of Human Biology, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North C3-168, Seattle, Washington 98109, USA

Correspondence to: David C. Page¹ Correspondence and requests for materials should be addressed to D.C.P. (Email: dcpage@wi.mit.edu).

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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 chromosome^1, 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 stasis^3, 4. These theories have been buttressed by partial sequence data from newly emergent plant and animal Y chromosomes^{5, 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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