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

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

70 Scopus citations

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 languageAmerican English
Pages (from-to)E2114-E2123
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number15
DOIs
StatePublished - 12 Apr 2016
Externally publishedYes

Bibliographical note

Funding Information:
Acknowledgments: We thank F. Catteruccia and S. N. Mitchell for sharing unpublished data; J. Pease for assistance with simulations; M. Kern, M. Menichelli, M. K. Lawniczak, I. Antoshechkin, T. Persampieri, R. Carballar, and R. D'Amato for technical assistance and discussion; and two anonymous reviewers for helpful suggestions. Genomic sequencing was funded in part by a grant from the Eck Institute for Global Health, University of Notre Dame. RNA-Seq was funded in part from a European Community Seventh Framework Programme (FP7/2007-2013) under Grant 228421 (INFRAVEC). Individual laboratories were funded as follows: National Institutes of Health Grants R01AI076584 (to N.J.B. and M.W.H.), R21AI112734 (to N.J.B. and S.J.E.), R21AI101459 (to N.J.B.), R21AI094289 and R21AI099528 (to I.V.S.), R21AI105575 (to Z.J.T.), and HHSN272200900039C (to S.J.E.); the Foundation of the National Institutes of Health through the VCTR program of the Grand Challenges in Global Health Initiative (to N.J.B., A. Crisanti, P.-A.P., and T.N.); European Commission and Regione Umbria Grant I-MOVE (to R.G., E.F., and P.-A.P.); Rita-Levi Montalcini Career Development Award (to P.-A.P.); Marie Curie Intra-European Fellowship for Career Development PIEFGA-273268 (to T.D.); European Research Council Grant 335724 (to N.W.); National Science Foundation Graduate Research Fellowship Grant DGE-1519168 (to A.B.H.); Department of Education Graduate Assistance in Areas of National Need Fellowship (to A. Steele); and Fralin Life Science Institute of Virginia Tech (to I.V.S. and Z.J.T.). This research was supported in part by the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health (to S.K. and A.M.P.). The contributions of N.H.B., J.H., and D.R. were funded under Agreement HSHQDC-07-C-00020 awarded by the Department of Homeland Security (DHS) Science and Technology Directorate for the management and operation of the National Biodefense Analysis and Countermeasures Center (NBACC), a Federally Funded Research and Development Center. The views and conclusions contained in this document are those of the authors and should not be interpreted as necessarily representing the official policies, either expressed or implied, of the US Department of Homeland Security. In no event shall the DHS, NBACC, or Battelle National Biodefense Institute (BNBI) have any responsibility or liability for any use, misuse, inability to use, or reliance upon the information contained herein. The Department of Homeland Security does not endorse any products or commercial services mentioned in this publication.

Keywords

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

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