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

J. F. Hughes, H. Skaletsky, T. Pyntikova, N. Koutseva, T. Raudsepp, L. G. Brown, D. W. Bellott, T.-J. Cho, S. Dugan-Rocha, Z. Khan, C. Kremitzki, C. Fronick, T. A. Graves-Lindsay, L. Fulton, W. C. Warren, R. K. Wilson, E. Owens, J. E. Womack, W. J. Murphy,  Genome Research,  2020.

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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