title: Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae.
abstract: Chemically defended plant tissues present formidable barriers to herbivores. Although mechanisms to resist plant defenses have been identified in ancient herbivorous lineages, adaptations to overcome plant defenses during transitions to herbivory remain relatively unexplored. The fly genus Scaptomyza is nested within the genus Drosophila and includes species that feed on the living tissue of mustard plants (Brassicaceae), yet this lineage is derived from microbe-feeding ancestors. We found that mustard-feeding Scaptomyza species and microbe-feeding Drosophila melanogaster detoxify mustard oils, the primary chemical defenses in the Brassicaceae, using the widely conserved mercapturic acid pathway. This detoxification strategy differs from other specialist herbivores of mustard plants, which possess derived mechanisms to obviate mustard oil formation. To investigate whether mustard feeding is coupled with evolution in the mercapturic acid pathway, we profiled functional and molecular evolutionary changes in the enzyme glutathione S-transferase D1 (GSTD1), which catalyzes the first step of the mercapturic acid pathway and is induced by mustard defense products in Scaptomyza. GSTD1 acquired elevated activity against mustard oils in one mustard-feeding Scaptomyza species in which GstD1 was duplicated. Structural analysis and mutagenesis revealed that substitutions at conserved residues within and near the substrate-binding cleft account for most of this increase in activity against mustard oils. Functional evolution of GSTD1 was coupled with signatures of episodic positive selection in GstD1 after the evolution of herbivory. Overall, we found that preexisting functions of generalized detoxification systems, and their refinement by natural selection, could play a central role in the evolution of herbivory.
authors: Department of Ecology and Evolutionary Biology, University of Arizona agloss@email.arizona.edu whiteman@email.arizona.edu.
authors: Andrew D
authors: AD
authors: Gloss
authors: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors: Daniel G
authors: DG
authors: Vassão
authors: Department of Chemistry and Biochemistry, University of Arizona.
authors: Alexander L
authors: AL
authors: Hailey
authors: Department of Ecology and Evolutionary Biology, University of Arizona.
authors: Anna C
authors: AC
authors: Nelson Dittrich
authors: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors: Katharina
authors: K
authors: Schramm
authors: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors: Michael
authors: M
authors: Reichelt
authors: Department of Ecology and Evolutionary Biology, University of Arizona.
authors: Timothy J
authors: TJ
authors: Rast
authors: Department of Chemistry and Biochemistry, University of Arizona.
authors: Andrzej
authors: A
authors: Weichsel
authors: Department of Ecology and Evolutionary Biology, University of Arizona.
authors: Matthew G
authors: MG
authors: Cravens
authors: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors: Jonathan
authors: J
authors: Gershenzon
authors: Department of Chemistry and Biochemistry, University of Arizona.
authors: William R
authors: WR
authors: Montfort
authors: Department of Ecology and Evolutionary Biology, University of Arizona agloss@email.arizona.edu whiteman@email.arizona.edu.
authors: Noah K
authors: NK
authors: Whiteman
mesh_terms: D000111:Acetylcysteine / Q000378:metabolism*; D000818:Animals; D018428:Drosophilidae / Q000145:classification / Q000235:genetics / Q000502:physiology*; D019143:Evolution, Molecular; D020440:Gene Duplication; D005982:Glutathione Transferase / Q000235:genetics* / Q000378:metabolism; D060434:Herbivory / Q000235:genetics; D019476:Insect Proteins / Q000235:genetics* / Q000378:metabolism; D009149:Mustard Plant / Q000737:chemistry / Q000378:metabolism*; D009154:Mutation; D010802:Phylogeny; D010938:Plant Oils / Q000378:metabolism*; D012641:Selection, Genetic; D015398:Signal Transduction
chemical_list: D019476:Insect Proteins; D010938:Plant Oils; D005982:Glutathione Transferase; C027793:mustard oil; D000111:Acetylcysteine
keywords: Drosophila; detoxification; gene duplication; glutathione S-transferase; isothiocyanate; plant–herbivore interactions