title: Genomics of ecological adaptation in cactophilic Drosophila.
abstract: Cactophilic Drosophila species provide a valuable model to study gene-environment interactions and ecological adaptation. Drosophila buzzatii and Drosophila mojavensis are two cactophilic species that belong to the repleta group, but have very different geographical distributions and primary host plants. To investigate the genomic basis of ecological adaptation, we sequenced the genome and developmental transcriptome of D. buzzatii and compared its gene content with that of D. mojavensis and two other noncactophilic Drosophila species in the same subgenus. The newly sequenced D. buzzatii genome (161.5 Mb) comprises 826 scaffolds (>3 kb) and contains 13,657 annotated protein-coding genes. Using RNA sequencing data of five life-stages we found expression of 15,026 genes, 80% protein-coding genes, and 20% noncoding RNA genes. In total, we detected 1,294 genes putatively under positive selection. Interestingly, among genes under positive selection in the D. mojavensis lineage, there is an excess of genes involved in metabolism of heterocyclic compounds that are abundant in Stenocereus cacti and toxic to nonresident Drosophila species. We found 117 orphan genes in the shared D. buzzatii-D. mojavensis lineage. In addition, gene duplication analysis identified lineage-specific expanded families with functional annotations associated with proteolysis, zinc ion binding, chitin binding, sensory perception, ethanol tolerance, immunity, physiology, and reproduction. In summary, we identified genetic signatures of adaptation in the shared D. buzzatii-D. mojavensis lineage, and in the two separate D. buzzatii and D. mojavensis lineages. Many of the novel lineage-specific genomic features are promising candidates for explaining the adaptation of these species to their distinct ecological niches.
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain.
authors.forename: Yolanda
authors.initials: Y
authors.lastname: Guillén
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain.
authors.forename: Núria
authors.initials: N
authors.lastname: Rius
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain.
authors.forename: Alejandra
authors.initials: A
authors.lastname: Delprat
authors.affiliation: Department of Biology, University of Texas at Arlington.
authors.forename: Anna
authors.initials: A
authors.lastname: Williford
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain.
authors.forename: Francesc
authors.initials: F
authors.lastname: Muyas
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain.
authors.forename: Marta
authors.initials: M
authors.lastname: Puig
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain Institut de Biotecnologia i de Biomedicina, Universitat Autònoma de Barcelona, Spain.
authors.forename: Sònia
authors.initials: S
authors.lastname: Casillas
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain Institut de Biotecnologia i de Biomedicina, Universitat Autònoma de Barcelona, Spain.
authors.forename: Miquel
authors.initials: M
authors.lastname: Ràmia
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain Institut de Biotecnologia i de Biomedicina, Universitat Autònoma de Barcelona, Spain.
authors.forename: Raquel
authors.initials: R
authors.lastname: Egea
authors.affiliation: EMBL/CRG Research Unit in Systems Biology, Centre for Genomic Regulation (CRG), Barcelona, Spain Universitat Pompeu Fabra (UPF), Barcelona, Spain.
authors.forename: Barbara
authors.initials: B
authors.lastname: Negre
authors.affiliation: IRTA, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB, Edifici CRAG, Barcelona, Spain The Peter MacCallum Cancer Centre, East Melbourne, Victoria, Australia.
authors.forename: Gisela
authors.initials: G
authors.lastname: Mir
authors.affiliation: Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Torre I, Barcelona, Spain.
authors.forename: Jordi
authors.initials: J
authors.lastname: Camps
authors.affiliation: Barcelona Supercomputing Center (BSC), Edifici TG (Torre Girona), Barcelona, Spain and Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.
authors.forename: Valentí
authors.initials: V
authors.lastname: Moncunill
authors.affiliation: Departamento de Genética, Facultad de Ciencias, Universidad de Granada, Spain.
authors.forename: Francisco J
authors.initials: FJ
authors.lastname: Ruiz-Ruano
authors.affiliation: Departamento de Genética, Facultad de Ciencias, Universidad de Granada, Spain.
authors.forename: Josefa
authors.initials: J
authors.lastname: Cabrero
authors.affiliation: Instituto de Ciências Biológicas, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil.
authors.forename: Leonardo G
authors.initials: LG
authors.lastname: de Lima
authors.affiliation: Instituto de Ciências Biológicas, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil.
authors.forename: Guilherme B
authors.initials: GB
authors.lastname: Dias
authors.affiliation: Informática de Biossistemas, Centro de Pesquisas René Rachou-Fiocruz Minas, Belo Horizonte, MG, Brazil.
authors.forename: Jeronimo C
authors.initials: JC
authors.lastname: Ruiz
authors.affiliation: Department of Human Genetics, University of Utah School of Medicine.
authors.forename: Aurélie
authors.initials: A
authors.lastname: Kapusta
authors.affiliation: IRTA, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB, Edifici CRAG, Barcelona, Spain.
authors.forename: Jordi
authors.initials: J
authors.lastname: Garcia-Mas
authors.affiliation: Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Torre I, Barcelona, Spain.
authors.forename: Marta
authors.initials: M
authors.lastname: Gut
authors.affiliation: Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Torre I, Barcelona, Spain.
authors.forename: Ivo G
authors.initials: IG
authors.lastname: Gut
authors.affiliation: Barcelona Supercomputing Center (BSC), Edifici TG (Torre Girona), Barcelona, Spain and Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.
authors.forename: David
authors.initials: D
authors.lastname: Torrents
authors.affiliation: Departamento de Genética, Facultad de Ciencias, Universidad de Granada, Spain.
authors.forename: Juan P
authors.initials: JP
authors.lastname: Camacho
authors.affiliation: Instituto de Ciências Biológicas, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil.
authors.forename: Gustavo C S
authors.initials: GC
authors.lastname: Kuhn
authors.affiliation: Department of Human Genetics, University of Utah School of Medicine.
authors.forename: Cédric
authors.initials: C
authors.lastname: Feschotte
authors.affiliation: Department of Molecular Biology and Genetics, Cornell University.
authors.forename: Andrew G
authors.initials: AG
authors.lastname: Clark
authors.affiliation: Department of Biology, University of Texas at Arlington.
authors.forename: Esther
authors.initials: E
authors.lastname: Betrán
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain Institut de Biotecnologia i de Biomedicina, Universitat Autònoma de Barcelona, Spain.
authors.forename: Antonio
authors.initials: A
authors.lastname: Barbadilla
authors.affiliation: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Spain alfredo.ruiz@uab.cat.
authors.forename: Alfredo
authors.initials: A
authors.lastname: Ruiz
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D029421:Cactaceae; D004330:Drosophila / Q000235:genetics* / Q000502:physiology; D017753:Ecosystem; D005786:Gene Expression Regulation; D049750:Genome, Insect; D023281:Genomics; D058977:Molecular Sequence Annotation; D016366:Open Reading Frames / Q000235:genetics; D017423:Sequence Analysis, RNA; D059467:Transcriptome / Q000235:genetics*
keywords: cactophilic Drosophila; ecological adaptation; gene duplication; genome sequence; orphan genes; positive selection