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Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages

    • 1Whitehead Institute, Cambridge, Massachusetts 02142, USA;
    • 2Howard Hughes Medical Institute, Whitehead Institute, Cambridge, Massachusetts 02142, USA;
    • 3College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas 77843, USA;
    • 4Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030, USA;
    • 5The McDonnell Genome Institute, Washington University School of Medicine, St. Louis, Missouri 63108, USA;
    • 6Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02142, USA
    • Present addresses: 7Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA; 8Institute for Genomic Medicine, Nationwide Children's Hospital, Columbus, OH 43205, USA; 9College of Food and Agriculture, United Arab Emirates University, Dubai, United Arab Emirates
Published November 18, 2020. https://doi.org/10.1101/gr.269902.120
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Abstract

Studies of Y Chromosome evolution have focused primarily on gene decay, a consequence of suppression of crossing-over with the X Chromosome. Here, we provide evidence that suppression of X–Y crossing-over unleashed a second dynamic: selfish X–Y arms races that reshaped the sex chromosomes in mammals as different as cattle, mice, and men. Using super-resolution sequencing, we explore the Y Chromosome of Bos taurus (bull) and find it to be dominated by massive, lineage-specific amplification of testis-expressed gene families, making it the most gene-dense Y Chromosome sequenced to date. As in mice, an X-linked homolog of a bull Y-amplified gene has become testis-specific and amplified. This evolutionary convergence implies that lineage-specific X–Y coevolution through gene amplification, and the selfish forces underlying this phenomenon, were dominatingly powerful among diverse mammalian lineages. Together with Y gene decay, X–Y arms races molded mammalian sex chromosomes and influenced the course of mammalian evolution.

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