Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet

Benjamin Goldman-Huertas, Robert F. Mitchell, Richard T. Lapoint, Cécile P. Faucher, John G Hildebrand, Noah K Whiteman

Research output: Contribution to journalArticle

54 Citations (Scopus)

Abstract

Herbivory is a key innovation in insects, yet has only evolved in onethird of living orders. The evolution of herbivory likely involves major behavioral changes mediated by remodeling of canonical chemosensory modules. Herbivorous flies in the genus Scaptomyza (Drosophilidae) are compelling species in which to study the genomic architecture linked to the transition to herbivory because they recently evolved from microbe-feeding ancestors and are closely related to Drosophila melanogaster. We found that Scaptomyza flava, a leaf-mining specialist on plants in the family (Brassicaceae), was not attracted to yeast volatiles in a four-field olfactometer assay, whereas D. melanogaster was strongly attracted to these volatiles. Yeast-associated volatiles, especially short-chain aliphatic esters, elicited strong antennal responses in D. melanogaster, but weak antennal responses in electroantennographic recordings from S. flava. We sequenced the genome of S. flava and characterized this species' odorant receptor repertoire. Orthologs of odorant receptors, which detect yeast volatiles in D. melanogaster and mediate critical host-choice behavior, were deleted or pseudogenized in the genome of S. flava . These genes were lost step-wise during the evolution of Scaptomyza. Additionally, Scaptomyza has experienced gene duplication and likely positive selection in paralogs of Or67b in D. melanogaster. Olfactory sensory neurons expressing Or67b are sensitive to green-leaf volatiles. Major trophic shifts in insects are associated with chemoreceptor gene loss as recently evolved ecologies shape sensory repertoires.

Original languageEnglish (US)
Pages (from-to)3026-3031
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number10
DOIs
StatePublished - Mar 10 2015

Fingerprint

Drosophilidae
Odorant Receptors
Herbivory
Drosophila melanogaster
Diet
Yeasts
Insects
Olfactory Receptor Neurons
Genome
Choice Behavior
Brassicaceae
Gene Duplication
Ecology
Diptera
Genes
Esters

Keywords

  • Drosophila melanogaster
  • Gene loss
  • Olfaction
  • Plant-herbivore interactions
  • Scaptomyza flava

ASJC Scopus subject areas

  • General

Cite this

Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet. / Goldman-Huertas, Benjamin; Mitchell, Robert F.; Lapoint, Richard T.; Faucher, Cécile P.; Hildebrand, John G; Whiteman, Noah K.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 10, 10.03.2015, p. 3026-3031.

Research output: Contribution to journalArticle

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