Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii
- Department of Molecular, Cellular and Developmental Biology, Yale University, United States
Figures
Figure 1
Oviposition preferences of Drosophila suzukii among a broad range of ripening stages.
(A) Phylogenetic tree depicting the relationship between D. suzukii and closely related Drosophila species. From http://spottedwingflybase.org/. (B) The multiple-choice oviposition assay. (C–E) …
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Figure 1—source data 1
Source data for number of eggs laid on each stage of ripening in Figure 1.
- https://cdn.elifesciences.org/articles/64317/elife-64317-fig1-data1-v1.xlsx
Figure 2
Taste contributes to the oviposition difference between Drosophila suzukii and Drosophila melanogaster.
(A) The two-choice oviposition assay. (B) Oviposition preferences of D. suzukii and D. melanogaster for ripe and overripe strawberry. *p<0.05, Mann-Whitney test, n = 7. The numbers of eggs laid were …
Figure 3 with 1 supplement
Taste sensilla on the labellum and leg.
(A) Scanning electron micrograph of the labellum of D. suzukii showing short taste sensilla (white dots), intermediate taste sensilla (white arrowheads), long taste sensilla (white arrows), and …
Figure 3—figure supplement 1
The ovipositor in Drosophila suzukii.
(A) Scanning electron micrograph of the ovipositor of D. suzukii showing bristles on each vaginal plate (VP). White arrowheads = thorn bristles type 1. White arrows and black arrowheads = thorn …
Figure 4 with 2 supplements
Electrophysiological responses to bitter compounds in labellar sensilla of the three Drosophila species.
For Drosophila suzukii, n = 5–10 for 84% of the 459 tastant-sensillum combinations; n > 10 for the remaining 16%. For Drosophila biarmipes, n = 5–10 for 96% of the 459 tastant-sensillum combinations;…
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Figure 4—source data 1
Responses to bitter compounds across species.
(A) Responses in spikes/s of labellar sensilla of three species to bitter compounds. Values represent the mean responses in spikes per second as measured by the number of action potentials generated over a 500 ms interval. For Drosophila suzukii, n = 5–10 for 84% of the 459 tastant-sensillum combinations; n > 10 for the remaining 16%. For Drosophila biarmipes, n = 5–10 for 96% of the 459 tastant-sensillum combinations; n > 10 for the remaining 4%. Responses to the tricholine citrate (TCC) diluent have been subtracted from the tastant responses. (B) SEMs of responses shown in (A). Data from Drosophila melanogaster are from Weiss et al., 2011.
- https://cdn.elifesciences.org/articles/64317/elife-64317-fig4-data1-v1.pdf
Figure 4—figure supplement 1
Dose response curves of caffeine (CAF), umbelliferone (UMB), and theophylline (TPH) from I8 in all three species.
Some values are too small to be seen.
Figure 4—figure supplement 2
Hierarchical cluster analysis, based on Ward's method, of labellar sensilla in Drosophila suzukii (A), Drosophila biarmipes (B), and Drosophila melanogaster (C).
The diluent control was subtracted from each response. Although the S-a and S-b sensilla occupy similar map positions in Drosophila simulans and D. biarmipes, there are two fewer S sensilla in these …
Figure 5
Sample electrophysiological traces from labellar sensilla of the three species.
(A) Escin (ESC) elicits strong responses from S9 in Drosophila suzukii and Drosophila biarmipes but a weak response from S10 in Drosophila melanogaster, which is at approximately the same position …
Figure 6 with 2 supplements
Strawberry extracts elicit different labellar responses from Drosophila suzukii than from other species.
(A) Labellar taste responses of Drosophila melanogaster, D. suzukii, and Drosophila biarmipes to ripe and overripe strawberry. The strawberry extracts were those used as stages 5 and 7 in the …
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Figure 6—source data 1
Source data for spike numbers in Figure 6.
- https://cdn.elifesciences.org/articles/64317/elife-64317-fig6-data1-v1.xlsx
Figure 6—figure supplement 1
Strawberry extracts elicit different labellar responses from Drosophila suzukii than from other species.
(A) Mean labellar responses of each functional class to ripe and overripe strawberry in all three species. Labellar taste responses of Drosophila melanogaster, D. suzukii, and Drosophila biarmipes …
Figure 6—figure supplement 2
All three species are distinguishable based on their responses to extracts of ripe and overripe strawberry.
Principal component analysis (PCA), calculated from labellar responses to extracts of ripe (A) or overripe strawberry (B).
Figure 7 with 1 supplement
Coding of bitter compounds in the female foreleg of Drosophila suzukii and related species.
(A) Heat map of electrophysiological responses to bitter compounds. n = 5–17. Responses to the diluent control, tricholine citrate (TCC), were subtracted. (B) Sample electrophysiological traces. …
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Figure 7—source data 1
Responses in spikes/s of tarsal sensilla of three species to bitter compounds.
Values represent the mean ± SEM responses of spikes/s. n = 5–17. Responses to the diluent control, tricholine citrate (TCC), were subtracted.
- https://cdn.elifesciences.org/articles/64317/elife-64317-fig7-data1-v1.pdf
Figure 7—figure supplement 1
Clustering of taste sensilla in the last two tarsal segments of the female foreleg into functional classes in all three species.
Figure 8
Drosophila suzukii oviposition is not deterred by bitter compounds that deter its close relatives.
(A) The two-choice oviposition assay. The oviposition preference is defined as: (number of eggs on sucrose substrate – number of eggs on sucrose+bitter substrate)/(total number of eggs on both …
Figure 9 with 3 supplements
Distinct labellar transcriptomes across the Drosophila species.
(A) Hierarchical clustering of the Drosophila melanogaster, Drosophila suzukii, and Drosophila biarmipes labellar transcriptomes. (B) Principal component analysis of the D. melanogaster, D. suzukii, …
Figure 9—figure supplement 1
Ionotropic receptor transcript detection in the labellum.
(A) Diagram of the Drosophila mouthparts and the labellar (blue) and pharyngeal (red) taste sensilla (adapted from Koh et al., 2014). (B) RNAseq coverage of typical labellar (blue) and pharyngeal …
Figure 9—figure supplement 2
Gustatory receptor (Gr) and odorant binding protein (Obp) expression in the labellum of Drosophila melanogaster.
D. melanogaster labellar expression level of Grs (A) and Obps (B) average FPKM values ≥0.5; detection in the labellum in previous studies (Galindo and Smith, 2001; Moon et al., 2009; Weiss et al., …
Figure 9—figure supplement 3
Gr22f is detected in Drosophila melanogaster and Drosophila biarmipes but not in Drosophila suzukii labella.
(A) RT-PCR (reverse transcription-polymerase chain reaction) analysis of Gr22f from labellar preparations of all three species. The same amount of RNA was used for RT-PCR amplification of elav …
Tables
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Strain (Drosophila melanogaster) | Canton-S | Koh et al., 2014 | NA | DOI:10.1016/j.neuron. 2014.07.012 |
| Strain (Drosophila melanogaster) | Canton-S w1118 | Koh et al., 2014 | NA | DOI:10.1016/j.neuron. 2014.07.012 |
| Strain (Drosophila melanogaster) | Gr33a2 | Dweck and Carlson, 2020 | NA | DOI:10.1016/j.cub.2019.11.005 |
| Strain (Drosophila melanogaster) | Gr33a3 | Dweck and Carlson, 2020 | NA | DOI:10.1016/j.cub.2019.11.005 |
| Strain (Drosophila biarmipes) | Dbia | Drosophila species stock center | 14023–0361.04 | Drosophila species stock center |
| Strain (Drosophila suzukii) | Dsuz | This paper | NA | Connecticut |
| Chemical compound | Aristolochic acid (ARI) | MilliporeSigma | Cat # A5512 | CAS # 313-67-7 |
| Chemical compound | Azadirachtin (AZA) | MilliporeSigma | Cat # A7430 | CAS # 11141-17-6 |
| Chemical compound | Berberine chloride (BER) | MilliporeSigma | Cat # Y0001149 | CAS # Y0001149 |
| Chemical compound | Caffeine (CAF) | MilliporeSigma | Cat # C1778 | CAS # 58-08-2 |
| Chemical compound | Coumarin (COU) | MilliporeSigma | Cat # C4261 | CAS # 91-64-5 |
| Chemical compound | N,N-Diethyl-meta- toluamide (DEET) | MilliporeSigma | Cat # 36542 | CAS # 134-62-3 |
| Chemical compound | Denatonium benzoate (DEN) | MilliporeSigma | Cat # D5765 | CAS # 3734-33-6 |
| Chemical compound | Escin (ESC) | MilliporeSigma | Cat # E1378 | CAS # 6805-41-0 |
| Chemical compound | (±)-Gossypol from cotton seeds (GOS) | MilliporeSigma | Cat # G8761 | CAS # 303-45-7 |
| Chemical compound | (-)-Lobeline hydrochloride (LOB) | MilliporeSigma | Cat # 141879 | CAS # 134-63-4 |
| Chemical compound | Saponin (SAP) | MilliporeSigma | Cat # 47036 | CAS # 8047-15-2 |
| Chemical compound | D-(+)-sucrose octaacetate (SOA) | MilliporeSigma | Cat # W303801 | CAS # 126-14-7 |
| Chemical compound | Sparteine sulfate salt (SPS) | MilliporeSigma | Cat# 234664 | CAS # 6160-12-9 |
| Chemical compound | Strychnine nitrate salt (STR) | MilliporeSigma | Cat # S2880 | CAS # 66-32-0 |
| Chemical compound | Theophylline (TPH) | MilliporeSigma | Cat # T1633 | CAS # 58-55-9 |
| Chemical compound | Tricholine citrate (TCC) | MilliporeSigma | Cat # T0252 | CAS # 546-63-4 |
| Chemical compound | Umbelliferone (UMB) | MilliporeSigma | Cat # H24003 | CAS # 93-35-6 |
Additional files
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Supplementary file 1
FPKM values for Drosophila melanogaster.
- https://cdn.elifesciences.org/articles/64317/elife-64317-supp1-v1.xlsx
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Supplementary file 2
TPM values for the three replicates of Drosophila melanogaster, Drosophila suzukii, and Drosophila biarmipes.
- https://cdn.elifesciences.org/articles/64317/elife-64317-supp2-v1.xlsx
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Supplementary file 3
DESeq2 differential gene expression analysis between Drosophila suzukii and Drosophila melanogaster.
Log2FCs are described in the 3rd column, adjusted p-values in the 6th column, and whether a gene was considered a hit in all four differential expression (DE) analysis pipelines (‘yes’) or not (‘no’).
- https://cdn.elifesciences.org/articles/64317/elife-64317-supp3-v1.xlsx
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Supplementary file 4
DESeq2 differential gene expression analysis between Drosophila suzukii and Drosophila biarmipes.
Log2FCs are described in the 3rd column, adjusted p-values in the 6th column, and whether a gene was considered a hit in all four differential expression (DE) analysis pipelines (yes) or not (no).
- https://cdn.elifesciences.org/articles/64317/elife-64317-supp4-v1.xlsx
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Transparent reporting form
- https://cdn.elifesciences.org/articles/64317/elife-64317-transrepform-v1.docx
