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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.

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Authors

Andrew Brantley Hall

Philippos-Aris Papathanos

Atashi Sharma

Changde Cheng

Omar S. Akbari

Lauren Assour

Nicholas H. Bergman

Alessia Cagnetti

Andrea Crisanti

Tania Dottorini

Elisa Fiorentini

Jonathan Hnath

Xiaofang Jiang

Sergey Koren

Tony Nolan

Diane Radune

Maria V. Sharakhova

Aaron Steele

Vladimir A. Timoshevskiy

Nikolai Windbichler

Simo Zhang

Matthew W. Hahn

Adam M. Phillippy

Scott J. Emrich

Igor V. Sharakhov

Zhijian Jake Tu

Nora J. Besansky



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.

Journal Article Type Article
Acceptance Date Mar 7, 2016
Publication Date Mar 29, 2016
Publicly Available Date Mar 28, 2024
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

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