Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

Julianne N Peláez; Andrew D Gloss; Benjamin Goldman-Huertas; Bernard Kim; Richard T Lapoint; Giovani Pimentel-Solorio; Kirsten I Verster; Jessica M Aguilar; Anna C Nelson Dittrich; Malvika Singhal; Hiromu C Suzuki; Teruyuki Matsunaga; Ellie E Armstrong; Joseph L M Charboneau; Simon C Groen; David H Hembry; Christopher J Ochoa; Timothy K O'Connor; Stefan Prost; Sophie Zaaijer; Paul D Nabity; Jiarui Wang; Esteban Rodas; Irene Liang; Noah K Whiteman

doi:10.1093/g3journal/jkad133

Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

G3 (Bethesda). 2023 Aug 9;13(8):jkad133. doi: 10.1093/g3journal/jkad133.

Authors

Julianne N Peláez^{1

2}, Andrew D Gloss^{3

4}, Benjamin Goldman-Huertas^{1

3}, Bernard Kim⁵, Richard T Lapoint^{3

6}, Giovani Pimentel-Solorio¹, Kirsten I Verster^{1

5}, Jessica M Aguilar¹, Anna C Nelson Dittrich^{3

7}, Malvika Singhal^{1

8}, Hiromu C Suzuki¹, Teruyuki Matsunaga¹, Ellie E Armstrong⁵, Joseph L M Charboneau³, Simon C Groen^{1

3

4

9

10

11}, David H Hembry^{3

12}, Christopher J Ochoa^{1

13}, Timothy K O'Connor¹, Stefan Prost^{1

5}, Sophie Zaaijer^{3

14

15}, Paul D Nabity^{3

10}, Jiarui Wang^{1

16}, Esteban Rodas¹, Irene Liang¹, Noah K Whiteman^{1

17}

Affiliations

¹ Department of Integrative Biology, University of California Berkeley, Berkeley, CA 94720, USA.
² Department of Biology, Brandeis University, Waltham, MA 02453, USA.
³ Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA.
⁴ Department of Biology and Center for Genomics and Systems Biology, New York University, New York, NY 10003, USA.
⁵ Department of Biology, Stanford University, Palo Alto, CA 94305, USA.
⁶ National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA.
⁷ Boyce Thompson Institute, Cornell University, Ithaca, NY 14853, USA.
⁸ Department of Chemistry & Biochemistry, University of Oregon, Eugene, OR 97403, USA.
⁹ Department of Nematology, University of California Riverside, Riverside, CA 92521, USA.
¹⁰ Department of Botany and Plant Sciences, University of California Riverside, Riverside, CA 92521, USA.
¹¹ Center for Plant Cell Biology and Institute for Integrative Genome Biology, University of California Riverside, Riverside, CA 92521, USA.
¹² Department of Biology, University of Texas Permian Basin, Odessa, TX 79762, USA.
¹³ Molecular Biology Institute, University of California Los Angeles, Los Angeles, CA 90095, USA.
¹⁴ Jacobs Institute, Cornell Tech, New York, NY 10044, USA.
¹⁵ FIND Genomics, New York, NY 10044, USA.
¹⁶ Department of Biomedical Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90007, USA.
¹⁷ Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, CA 94720, USA.

Abstract

Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genomic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families-genes directly mediating interactions with plant chemical defenses-underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many insect lineages are ancient (>150 million years ago (mya)), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several nonherbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza has among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant-binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on living plants (bitter or electrophilic phytotoxins) or their ancestral diet (fermenting plant volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight gene candidates that have also been linked to other dietary transitions in Drosophila.

Keywords: Drosophila; Scaptomyza; adaptation; gene family evolution; genomics; plant-herbivore interactions; trophic shift.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Drosophila / genetics
Drosophila / metabolism
Drosophila Proteins* / genetics
Evolution, Molecular
Genomics / methods
Herbivory* / genetics
Insecta
Phylogeny

Substances

Drosophila Proteins

Grants and funding

R35 GM119816/GM/NIGMS NIH HHS/United States