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

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, Roberto Galizi, Jonathan Hnath, Xiaofang Jiang, Sergey Koren, Tony Nolan, Diane Radune, Maria V. Sharakhova, Aaron Steele, Vladimir A. TimoshevskiyNikolai Windbichler, Simo Zhang, Matthew W. Hahn, Adam M. Phillippy, Scott J. Emrich, Igor V. Sharakhov, Zhijian Jake Tu, Nora J. Besansky

Research output: Journal PublicationArticlepeer-review

61 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)E2114-E2123
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number15
DOIs
Publication statusPublished - 12 Apr 2016
Externally publishedYes

Keywords

  • Anopheles gambiae
  • Pacbio
  • RNA-Seq
  • Tandem repetitive DNA
  • Y-chromosome

ASJC Scopus subject areas

  • General

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