Meiotic Executioner Genes Protect the Y from Extinction

• Published in: Trends in genetics Vol. 36; no. 10; pp. 728 - 738
• Main Authors: Waters, Paul D., Ruiz-Herrera, Aurora
• Format: Journal Article
• Language: English
• Published: Elsevier Ltd 01.10.2020
• Subjects: executioner genes; meiosis; meiotic sex chromosome inactivation; sex chromosome evolution; Y chromosome loss; Zfy; Y chromosome loss; executioner genes; meiotic sex chromosome inactivation; meiosis; Zfy; sex chromosome evolution
• ISSN: 0168-9525
• DOI: 10.1016/j.tig.2020.06.008

The Y has been described as a wimpy degraded relic of the X, with imminent demise should it lose sex-determining function. Why then has it persisted in almost all mammals? Here we present a novel mechanistic explanation for its evolutionary perseverance: the persistent Y hypothesis. The Y chromosome bears genes that act as their own judge, jury, and executioner in the tightly regulated meiotic surveillance pathways. These executioners are crucial for successful meiosis, yet need to be silenced during the meiotic sex chromosome inactivation window, otherwise germ cells die. Only rare transposition events to the X, where they remain subject to obligate meiotic silencing, are heritable, posing strong evolutionary constraint for the Y chromosome to persist. The mammalian Y chromosome has been proposed to be a wimp with impending demise should it lose sex-determining function.Changes in sex-determining switches are common in non-mammalian vertebrates, so an alternative explanation is required to explain Y chromosome persistence.The Y chromosome bears executioner genes that are essential for male meiosis, but must themselves also be subjected to meiotic silencing because they are pachytene lethal.The only heritable location that executioner genes can transpose to is the X chromosome (just 5% of the genome), where they remain subject to appropriate meiotic silencing.Transposition of executioner genes away from the Y chromosome is uncommon, posing strong evolutionary constraint for the Y to persistent.