title: Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes.
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.
authors.affiliation: The Interdisciplinary PhD Program in Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061;
authors.forename: Andrew Brantley
authors.initials: AB
authors.lastname: Hall
authors.affiliation: Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy; Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
authors.forename: Philippos-Aris
authors.initials: PA
authors.lastname: Papathanos
authors.affiliation: Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061;
authors.forename: Atashi
authors.initials: A
authors.lastname: Sharma
authors.affiliation: Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556;
authors.forename: Changde
authors.initials: C
authors.lastname: Cheng
authors.affiliation: Department of Entomology, Riverside Center for Disease Vector Research, Institute for Integrative Genome Biology, University of California, Riverside, CA 92521;
authors.forename: Omar S
authors.initials: OS
authors.lastname: Akbari
authors.affiliation: Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556;
authors.forename: Lauren
authors.initials: L
authors.lastname: Assour
authors.affiliation: National Biodefense Analysis and Countermeasures Center, Frederick, MD 21702;
authors.forename: Nicholas H
authors.initials: NH
authors.lastname: Bergman
authors.affiliation: Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy;
authors.forename: Alessia
authors.initials: A
authors.lastname: Cagnetti
authors.affiliation: Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy; Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
authors.forename: Andrea
authors.initials: A
authors.lastname: Crisanti
authors.affiliation: Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
authors.forename: Tania
authors.initials: T
authors.lastname: Dottorini
authors.affiliation: Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
authors.forename: Elisa
authors.initials: E
authors.lastname: Fiorentini
authors.affiliation: Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
authors.forename: Roberto
authors.initials: R
authors.lastname: Galizi
authors.affiliation: National Biodefense Analysis and Countermeasures Center, Frederick, MD 21702;
authors.forename: Jonathan
authors.initials: J
authors.lastname: Hnath
authors.affiliation: The Interdisciplinary PhD Program in Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061;
authors.forename: Xiaofang
authors.initials: X
authors.lastname: Jiang
authors.affiliation: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892;
authors.forename: Sergey
authors.initials: S
authors.lastname: Koren
authors.affiliation: Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
authors.forename: Tony
authors.initials: T
authors.lastname: Nolan
authors.affiliation: National Biodefense Analysis and Countermeasures Center, Frederick, MD 21702;
authors.forename: Diane
authors.initials: D
authors.lastname: Radune
authors.affiliation: Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Laboratory of Evolutionary Cytogenetics, Tomsk State University, Tomsk 634050, Russia;
authors.forename: Maria V
authors.initials: MV
authors.lastname: Sharakhova
authors.affiliation: Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556;
authors.forename: Aaron
authors.initials: A
authors.lastname: Steele
authors.affiliation: Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061;
authors.forename: Vladimir A
authors.initials: VA
authors.lastname: Timoshevskiy
authors.affiliation: Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
authors.forename: Nikolai
authors.initials: N
authors.lastname: Windbichler
authors.affiliation: School of Informatics and Computing, Indiana University, Bloomington, IN 47405;
authors.forename: Simo
authors.initials: S
authors.lastname: Zhang
authors.affiliation: School of Informatics and Computing, Indiana University, Bloomington, IN 47405; Department of Biology, Indiana University, Bloomington, IN 47405;
authors.forename: Matthew W
authors.identifier: http://orcid.org/0000-0002-5731-8808
authors.initials: MW
authors.lastname: Hahn
authors.affiliation: Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892;
authors.forename: Adam M
authors.identifier: http://orcid.org/0000-0003-2983-8934
authors.initials: AM
authors.lastname: Phillippy
authors.affiliation: Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556; Department of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556;
authors.forename: Scott J
authors.initials: SJ
authors.lastname: Emrich
authors.affiliation: The Interdisciplinary PhD Program in Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Laboratory of Evolutionary Cytogenetics, Tomsk State University, Tomsk 634050, Russia; igor@vt.edu jaketu@vt.edu nbesansk@nd.edu.
authors.forename: Igor V
authors.initials: IV
authors.lastname: Sharakhov
authors.affiliation: The Interdisciplinary PhD Program in Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 igor@vt.edu jaketu@vt.edu nbesansk@nd.edu.
authors.forename: Zhijian Jake
authors.initials: ZJ
authors.lastname: Tu
authors.affiliation: Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556; igor@vt.edu jaketu@vt.edu nbesansk@nd.edu.
authors.forename: Nora J
authors.initials: NJ
authors.lastname: Besansky
mesh_terms: D000818:Animals; D000852:Anopheles / Q000235:genetics*; D059006:Chromosomes, Insect / Q000235:genetics*; D005260:Female; D007303:Insect Vectors / Q000235:genetics*; D008288:Malaria; D008297:Male; D010802:Phylogeny; D017422:Sequence Analysis, DNA; D014960:X Chromosome / Q000235:genetics; D014998:Y Chromosome / Q000235:genetics*
keywords: Anopheles gambiae; PacBio; RNA-Seq; Y-chromosome; tandem repetitive DNA