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Proc Natl Acad Sci U S A. 2015 Mar 10;112(10):3026-31. doi: 10.1073/pnas.1424656112. Epub 2015 Jan 26.

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

Author information

1
Departments of Ecology and Evolutionary Biology and.
2
Neuroscience, and Center for Insect Science, University of Arizona, Tucson, AZ 85721; and.
3
Departments of Ecology and Evolutionary Biology and Center for Insect Science, University of Arizona, Tucson, AZ 85721; and.
4
Neuroscience, and Life Science Solutions, Thermo Fisher Scientific, 64293 Darmstadt, Germany.
5
Neuroscience, and jhildebr@email.arizona.edu whiteman@email.arizona.edu.
6
Departments of Ecology and Evolutionary Biology and jhildebr@email.arizona.edu whiteman@email.arizona.edu.

Abstract

Herbivory is a key innovation in insects, yet has only evolved in one-third 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.

KEYWORDS:

Drosophila melanogaster; Scaptomyza flava; gene loss; olfaction; plant–herbivore interactions

PMID:
25624509
PMCID:
PMC4364187
DOI:
10.1073/pnas.1424656112
[Indexed for MEDLINE]
Free PMC Article

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