Evolution of herbivory remodels aDrosophilagenome
Authors: Gloss Andrew D. , Nelson Dittrich Anna C. , Lapoint Richard T. , Goldman-Huertas Benjamin , Verster Kirsten I. , Pelaez Julianne L. , Nelson Andrew D. L. , Aguilar Jessica , Armstrong Ellie , Charboneau Joseph L.M. , Groen Simon C. , Hembry David H. , Ochoa Christopher J. , O’Connor Timothy K. , Prost Stefan , Suzuki Hiromu C. , Zaaijer Sophie , Nabity Paul. D. , Whiteman Noah K. 
Published: September 2019

One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, includingArabidopsis thaliana) in the fly genusScaptomyza,nested within the paraphyletic genusDrosophila. We discovered a radiation of mustard-specializedScaptomyzaspecies, comparable in diversity to theDrosophila melanogasterspecies subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species,S. flava,revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains (“blooms”) were found in Phase I and Phase II detoxification gene sub-families, including glutathioneS-transferase (Gst) and cytochrome P450 (Cyp450) genes.S. flavahas more validated paralogs of a singleCyp450(N=6 forCyp6g1) andGst(N=5 forGstE5-8) than any other drosophilid. Functional studies of theGstrepertoire inS. flavashowed that transcription ofS. flava GstE5-8paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolicS. flavaGST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxificationin vitro.One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms,DrosophilaandArabidopsis,helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.

SIGNIFICANCE STATEMENT

The origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly (Drosophila melanogaster), the “wasabi fly” (Scaptomyza flava), that evolved to consume mustard plants includingArabidopsis thaliana. The yeast-to-mustard dietary transition remodeled the fly’s gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals.