Skip to main content
bioRxiv
  • Home
  • About
  • Submit
  • ALERTS / RSS
Advanced Search
New Results

Evolution of herbivory remodels a Drosophila genome

Andrew D. Gloss, Anna C. Nelson Dittrich, Richard T. Lapoint, Benjamin Goldman-Huertas, Kirsten I. Verster, Julianne L. Pelaez, Andrew D. L. Nelson, Jessica Aguilar, Ellie Armstrong, Joseph L.M. Charboneau, Simon C. Groen, David H. Hembry, Christopher J. Ochoa, Timothy K. O’Connor, Stefan Prost, Hiromu C. Suzuki, Sophie Zaaijer, Paul. D. Nabity, View ORCID ProfileNoah K. Whiteman
doi: https://doi.org/10.1101/767160
Andrew D. Gloss
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USADepartment of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USADepartment of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: agloss@uchicago.edu whiteman@berkeley.edu
Anna C. Nelson Dittrich
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Richard T. Lapoint
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USANational Center for Biotechnology Information, Bethesda, MD 20894, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Benjamin Goldman-Huertas
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USADepartment of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kirsten I. Verster
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Julianne L. Pelaez
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Andrew D. L. Nelson
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jessica Aguilar
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ellie Armstrong
Department of Biology, Stanford University, Palo Alto, CA 94305, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Joseph L.M. Charboneau
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Simon C. Groen
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USADepartment of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USACenter for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
David H. Hembry
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Christopher J. Ochoa
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Timothy K. O’Connor
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USADepartment of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stefan Prost
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USADepartment of Biology, Stanford University, Palo Alto, CA 94305, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hiromu C. Suzuki
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sophie Zaaijer
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USAJacobs Institute, Cornell Tech, New York, NY 10044, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Paul. D. Nabity
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USADepartment of Botany and Plant Sciences, University of California-Riverside, Riverside, CA 92521, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Noah K. Whiteman
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Noah K. Whiteman
  • For correspondence: agloss@uchicago.edu whiteman@berkeley.edu
  • Abstract
  • Full Text
  • Info/History
  • Metrics
  • Supplementary material
  • Preview PDF
Loading

ABSTRACT

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, including Arabidopsis thaliana) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila. We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species 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 glutathione S-transferase (Gst) and cytochrome P450 (Cyp450) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1) and Gst (N=5 for GstE5-8) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in 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, Drosophila and Arabidopsis, 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 including Arabidopsis 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.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
Back to top
PreviousNext
Posted September 12, 2019.
Download PDF

Supplementary Material

Email

Thank you for your interest in spreading the word about bioRxiv.

NOTE: Your email address is requested solely to identify you as the sender of this article.

Enter multiple addresses on separate lines or separate them with commas.
Evolution of herbivory remodels a Drosophila genome
(Your Name) has forwarded a page to you from bioRxiv
(Your Name) thought you would like to see this page from the bioRxiv website.
Share
Evolution of herbivory remodels a Drosophila genome
Andrew D. Gloss, Anna C. Nelson Dittrich, Richard T. Lapoint, Benjamin Goldman-Huertas, Kirsten I. Verster, Julianne L. Pelaez, Andrew D. L. Nelson, Jessica Aguilar, Ellie Armstrong, Joseph L.M. Charboneau, Simon C. Groen, David H. Hembry, Christopher J. Ochoa, Timothy K. O’Connor, Stefan Prost, Hiromu C. Suzuki, Sophie Zaaijer, Paul. D. Nabity, Noah K. Whiteman
bioRxiv 767160; doi: https://doi.org/10.1101/767160
Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Evolution of herbivory remodels a Drosophila genome
Andrew D. Gloss, Anna C. Nelson Dittrich, Richard T. Lapoint, Benjamin Goldman-Huertas, Kirsten I. Verster, Julianne L. Pelaez, Andrew D. L. Nelson, Jessica Aguilar, Ellie Armstrong, Joseph L.M. Charboneau, Simon C. Groen, David H. Hembry, Christopher J. Ochoa, Timothy K. O’Connor, Stefan Prost, Hiromu C. Suzuki, Sophie Zaaijer, Paul. D. Nabity, Noah K. Whiteman
bioRxiv 767160; doi: https://doi.org/10.1101/767160

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Subject Area

  • Evolutionary Biology
Subject Areas
All Articles
  • Animal Behavior and Cognition (1529)
  • Biochemistry (2482)
  • Bioengineering (1742)
  • Bioinformatics (9687)
  • Biophysics (3907)
  • Cancer Biology (2974)
  • Cell Biology (4199)
  • Clinical Trials (135)
  • Developmental Biology (2635)
  • Ecology (4104)
  • Epidemiology (2033)
  • Evolutionary Biology (6902)
  • Genetics (5211)
  • Genomics (6508)
  • Immunology (2188)
  • Microbiology (6954)
  • Molecular Biology (2757)
  • Neuroscience (17316)
  • Paleontology (126)
  • Pathology (428)
  • Pharmacology and Toxicology (707)
  • Physiology (1058)
  • Plant Biology (2491)
  • Scientific Communication and Education (645)
  • Synthetic Biology (831)
  • Systems Biology (2690)
  • Zoology (430)