title: The making of a pest: Insights from the evolution of chemosensory receptor families in a pestiferous and invasive fly, Drosophila suzukii.
abstract: Drosophila suzukii differs from other melanogaster group members in their proclivity for laying eggs in fresh fruit rather than in fermenting fruits. Olfaction and gustation play a critical role during insect niche formation, and these senses are largely mediated by two important receptor families: olfactory and gustatory receptors (Ors and Grs). Earlier work from our laboratory has revealed how the olfactory landscape of D. suzukii is dominated by volatiles derived from its unique niche. Signaling and reception evolve in synchrony, since the interaction of ligands and receptors together mediate the chemosensory behavior. Here, we manually annotated the Ors and Grs in D. suzukii and two close relatives, D. biarmipes and D. takahashii, and compared these repertoires to those in other melanogaster group drosophilids to identify candidate chemoreceptors associated with D. suzukii's unusual niche utilization.
  
  
  
  Our comprehensive annotations of the chemosensory genomes in three species, and comparative analysis with other melanogaster group members provide insights into the evolution of chemosensation in the pestiferous D. suzukii. We annotated a total of 71 Or genes in D. suzukii, with nine of those being pseudogenes (12.7 %). Alternative splicing of two genes brings the total to 62 genes encoding 66 Ors. Duplications of Or23a and Or67a expanded D. suzukii's Or repertoire, while pseudogenization of Or74a, Or85a, and Or98b reduced the number of functional Ors to roughly the same as other annotated species in the melanogaster group. Seventy-one intact Gr genes and three pseudogenes were annotated in D. suzukii. Alternative splicing in three genes brings the total number of Grs to 81. We identified signatures of positive selection in two Ors and three Grs at nodes leading to D. suzukii, while three copies in the largest expanded Or lineage, Or67a, also showed signs of positive selection at the external nodes.
  
  
  
  Our analysis of D. suzukii's chemoreceptor repertoires in the context of nine melanogaster group drosophilids, including two of its closest relatives (D. biarmipes and D. takahashii), revealed several candidate receptors associated with the adaptation of D. suzukii to its unique ecological niche.
authors.affiliation: Department of Biological Sciences & Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, 46556, USA.
authors.forename: Paul V
authors.initials: PV
authors.lastname: Hickner
authors.affiliation: Department of Biological Sciences & Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, 46556, USA.
authors.forename: Chissa L
authors.initials: CL
authors.lastname: Rivaldi
authors.affiliation: Department of Biological Sciences & Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, 46556, USA.
authors.forename: Cole M
authors.initials: CM
authors.lastname: Johnson
authors.affiliation: Department of Biological Sciences & Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, 46556, USA.
authors.forename: Madhura
authors.initials: M
authors.lastname: Siddappaji
authors.affiliation: Department of Biological Sciences & Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, 46556, USA.
authors.forename: Gregory J
authors.initials: GJ
authors.lastname: Raster
authors.affiliation: Department of Biological Sciences & Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, 46556, USA. zainulabeuddin.syed.5@nd.edu.
authors.forename: Zainulabeuddin
authors.identifier: 0000-0002-6235-7115
authors.initials: Z
authors.lastname: Syed
mesh_terms: D000818:Animals; D005075:Biological Evolution; D004330:Drosophila / Q000235:genetics* / Q000648:ultrastructure; D029721:Drosophila Proteins / Q000737:chemistry / Q000235:genetics*; D019143:Evolution, Molecular; D005810:Multigene Family; D010802:Phylogeny; D011956:Receptors, Cell Surface / Q000737:chemistry / Q000235:genetics*; D018035:Receptors, Odorant / Q000737:chemistry / Q000235:genetics*; D012641:Selection, Genetic; D011984:Sensory Receptor Cells / Q000378:metabolism / Q000648:ultrastructure; D013045:Species Specificity
chemical_list: D029721:Drosophila Proteins; D011956:Receptors, Cell Surface; D018035:Receptors, Odorant; C405956:gustatory receptor, Drosophila
keywords: Adaption; Episodic selection; Gustation; Gustatory receptors; Molecular evolution; Niche utilization; Odorant receptors; Olfaction