Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes.

Brantley Hall, Andrew; Papathanos, Philippos-Aris; Sharma, Atashi; Cheng, Changde; Akbari, Omar S.; Assour, Lauren; Bergman, Nicholas H.; Cagnetti, Alessia; Crisanti, Andrea; Dottorini, Tania; Fiorentini, Elisa; Galizi, Roberto; Hnath, Jonathan; Jiang, Xiaofang; Koren, Sergey; Nolan, Tony; Radune, Diane; Sharakhova, Maria V.; Steele, Aaron; Timoshevskiy, Vladimir A.; Windbichler, Nikolai; Zhang, Simo; Hahn, Matthew W.; Phillippy, Adam M.; Emrich, Scott J.; Sharakhov, Igor V.; Jake Tu, Zhijian; Besansky, Nora J.

Abstract

Y chromosomes control essential male functions in many species, including sex determination and fertility. However, because of obstacles posed by repeat-rich heterochromatin, knowledge of Y chromosome sequences is limited to a handful of model organisms, constraining our understanding of Y biology across the tree of life. Here, we leverage long single-molecule sequencing to determine the content and structure of the nonrecombining Y chromosome of the primary African malaria mosquito, Anopheles gambiae We find that the An. gambiae Y consists almost entirely of a few massively amplified, tandemly arrayed repeats, some of which can recombine with similar repeats on the X chromosome. Sex-specific genome resequencing in a recent species radiation, the An. gambiae complex, revealed rapid sequence turnover within An. gambiae and among species. Exploiting 52 sex-specific An. gambiae RNA-Seq datasets representing all developmental stages, we identified a small repertoire of Y-linked genes that lack X gametologs and are not Y-linked in any other species except An. gambiae, with the notable exception of YG2, a candidate male-determining gene. YG2 is the only gene conserved and exclusive to the Y in all species examined, yet sequence similarity to YG2 is not detectable in the genome of a more distant mosquito relative, suggesting rapid evolution of Y chromosome genes in this highly dynamic genus of malaria vectors. The extensive characterization of the An. gambiae Y provides a long-awaited foundation for studying male mosquito biology, and will inform novel mosquito control strategies based on the manipulation of Y chromosomes.

Citation

Brantley Hall, A., Papathanos, P., Sharma, A., Cheng, C., Akbari, O. S., Assour, L., …Besansky, N. J. (2016). Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes. Proceedings of the National Academy of Sciences of the United States of America, E2114 - E2123. https://doi.org/10.1073/pnas.1525164113

• Journal Article Type: Article
• Acceptance Date: Mar 7, 2016
• Publication Date: Mar 29, 2016
• Journal: Proc Natl Acad Sci U S A
• Print ISSN: 1091-6490
• Publisher: National Academy of Sciences
• Pages: E2114 - E2123
• DOI: https://doi.org/10.1073/pnas.1525164113
• Keywords: Y Chromosome, Malaria, Mosquitoes
• Publisher URL: https://www.pnas.org/content/113/15/E2114/tab-article-info
• PMID: 27035980