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

Jennifer F. Hughes; Helen Skaletsky; Tatyana Pyntikova; Natalia Koutseva; Terje Raudsepp; Laura G. Brown; Daniel W. Bellott; Ting-Jan Cho; Shannon Dugan-Rocha; Ziad Khan; Colin Kremitzki; Catrina Fronick; Tina A. Graves-Lindsay; Lucinda Fulton; Wesley C. Warren; Richard K. Wilson; Elaine Owens; James E. Womack; William J. Murphy; Donna M. Muzny; Kim C. Worley; Bhanu P. Chowdhary; Richard A. Gibbs; David C. Page

doi:10.1101/gr.269902.120

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

Corresponding author: jhughes{at}wi.mit.edu

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.

Footnotes

[Supplemental material is available for this article.]
Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.269902.120.

Received August 6, 2020.
Accepted October 28, 2020.

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