Genes involved in the evolution of herbivory by a leaf-mining, drosophilid fly

Noah K. Whiteman, Andrew D. Gloss, Timothy B. Sackton, Simon C. Groen, Parris T. Humphrey, Richard T. Lapoint, Ida E. Sønderby, Barbara A. Halkier, Christine Kocks, Frederick M. Ausubel, Naomi E. Pierce

Research output: Contribution to journalArticle

35 Scopus citations

Abstract

Herbivorous insects are among the most successful radiations of life. However, we know little about the processes underpinning the evolution of herbivory. We examined the evolution of herbivory in the fly, Scaptomyza flava, whose larvae are leaf miners on species of Brassicaceae, including the widely studied reference plant, Arabidopsis thaliana (Arabidopsis). Scaptomyza flava is phylogenetically nested within the paraphyletic genus Drosophila, and the whole genome sequences available for 12 species of Drosophila facilitated phylogenetic analysis and assembly of a transcriptome for S. flava. A time-calibrated phylogeny indicated that leaf mining in Scaptomyza evolved between 6 and 16 million years ago. Feeding assays showed that biosynthesis of glucosinolates, the major class of antiherbivore chemical defense compounds in mustard leaves, was upregulated by S. flava larval feeding. The presence of glucosinolates in wild-type (WT) Arabidopsis plants reduced S. flava larval weight gain and increased egg-adult development time relative to flies reared in glucosinolate knockout (GKO)plants. Ananalysis of gene expression differences in 5-day-old larvae reared on WT versus GKO plants showed a total of 341 transcripts that were differentially regulated by glucosinolate uptake in larval S. flava. Of these, approximately a third corresponded to homologs of Drosophila melanogaster genes associated with starvation, dietary toxin-, heat-, oxidation-, and aging-related stress. The upregulated transcripts exhibited elevated rates of protein evolution compared with unregulated transcripts. There maining differentially regulated transcripts also contained a higher proportion of novelgenes than the unregulated transcripts. Thus, the transition to herbivory in Scaptomyza appears to be coupled with the evolution of novel genes and the co-option of conserved stress-related genes.

Original languageEnglish (US)
Pages (from-to)900-916
Number of pages17
JournalGenome biology and evolution
Volume4
Issue number9
DOIs
StatePublished - Dec 1 2012

Keywords

  • Arabidopsis
  • Drosophila
  • Glucosinolates
  • Herbivory
  • Host specialization
  • Transcriptome

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

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    Whiteman, N. K., Gloss, A. D., Sackton, T. B., Groen, S. C., Humphrey, P. T., Lapoint, R. T., Sønderby, I. E., Halkier, B. A., Kocks, C., Ausubel, F. M., & Pierce, N. E. (2012). Genes involved in the evolution of herbivory by a leaf-mining, drosophilid fly. Genome biology and evolution, 4(9), 900-916. https://doi.org/10.1093/gbe/evs063