Coordinated molecular and ecological adaptations underlie a highly successful parasitoid
- Institute of Insect Sciences, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, College of Agriculture and Biotechnology, Zhejiang University, China
- CAS Key Laboratory of Insect Developmental and Evolutionary Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, China
- CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, China
- Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Zhejiang University, China
- State Key Lab of Rice Biology, Zhejiang University, China
Figures
Figure 1 with 3 supplements
Chromosome-level assembly of a generalist drosophilid parasitoid genome.
(A) The life cycle of T. drosophilae (parasitoid) and Drosophila (host). T. drosophila (Td) is a pupal parasitoid that deposits eggs into Drosophila host pupae. As a generalist parasitoid, Td can …
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Figure 1—source data 1
Related to Figure 1B.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig1-data1-v1.xlsx
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Figure 1—source data 2
Related to Figure 1C.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig1-data2-v1.xlsx
Figure 1—figure supplement 1
Chromosome features of Trichopria drosophilae (Td).
(A) Chromosome staining of male Td haploid chromosome (n=6). Scale bars: 10 μm. (B) Chromosome staining of female Td diploid chromosome sets (2n=12). Scale bars: 10 μm. (C) The heatmap of Hi-C …
Figure 1—figure supplement 2
Distribution of repeat content among representative parasitoid species.
The age and relative abundance of repeat element classes across representative parasitoid genomes. The CpG-adjusted Kimura divergence from the consensus was estimated to indicate the time of …
Figure 1—figure supplement 3
Phylogeny and ortholog content across representative parasitoid species.
The phylogeny on the left is a maximum-likelihood phylogenetic tree based 1246 single-copy orthologs across 12 representative species with high-quality reference genomes as well we two related …
Figure 2
Genomic distribution and expression profiling of Timps in Trichopria drosophilae (Td).
(A) Top 20 expanded functional domains in Td genome in comparison to other parasitoids. Species abbreviations correspond to those in Figure 1D. (B) Genomic locations of characterized …
Figure 3 with 3 supplements
Trichopria drosophilae (Td) venom glands recruit a family of metalloproteinases (Timp) as venom proteins to arrest the host development.
(A) Schematic diagram of Td parasitization and venom injection into Drosophila host pupa. Wasp venom is produced in the venom gland (VG) and stored in the venom reservoir (VR). (B) and (C) …
Figure 3—figure supplement 1
Characterization of the developmental delay phenotype in Figure 3B (A) and Figure 3C (B).
The eye colours of Drosophila hosts were divided into ive levels from white (young) to red (old), including white, light orange, orange, light red, and red. The percentage of D. suzukii (A) and D. …
Figure 3—figure supplement 2
Development of D. melanogaster UAS-controls.
The UAS-controls for Figure 3F, including UAS-DmTimp, UAS-TdTimp1, UAS-TdTimp2, and UAS-TdTimp1 +TdTimp2. Fly eyes are marked by red arrowheads, and bristles are marked by yellow arrowheads. The …
Figure 3—figure supplement 3
Characterization of the developmental delay phenotype in Figure 3F and Figure 3—figure supplement 2.
The eye colours of D. melanogaster were divided into 5 levels from white (young) to red (old), including white, light orange, orange, light red, and red. The percentage of D. melanogaster pupae with …
Figure 4 with 5 supplements
Trichopria drosophilae (Td) teratocytes secret trypsin proteins to digest host tissues.
(A) Schematic diagram of teratocytes in Td-parasitized Drosophila hosts. Teratocytes are derived from the serosal membrane during Td egg hatching. (B) Transmission electron microscopy of Td …
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Figure 4—source data 1
Related to Figure 4F.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig4-data1-v1.xlsx
Figure 4—figure supplement 1
The teratocytes are released during Trichopria drosophilae (Td) egg hatching.
A Td egg was dissected and cultured in Schneider’s medium (Thermo Fisher Scientific, Cat#21720001). When the egg hatched into a larva in the culture medium, it released teratocytes as well. Scale …
Figure 4—figure supplement 2
The size and number of teratocytes in parasitized hosts.
(A) The teratocyte numbers in single D. suzukii host of different days post Trichopria drosophilae (Td) parasitization. n=31 for each group. (B) The teratocyte diameters in D. suzukii host of …
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Figure 4—figure supplement 2—source data 1
Related to Figure 4—figure supplement 2A.
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Figure 4—figure supplement 2—source data 2
Related to Figure 4—figure supplement 2B.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig4-figsupp2-data2-v1.xlsx
Figure 4—figure supplement 3
A trypsin inhibitor, TLCK, impairs the degradation function of teratocyte.
The percentage of host tissue at different digestion status in Figure 4E after incubation with a trypsin inhibitor, TLCK. Significance of the proportion of full digestion was analyzed by Fisher’s …
Figure 4—figure supplement 4
A trypsin inhibitor, TPCK, impairs the degradation function of teratocyte.
(A) Different concentrations of a trypsin inhibitor, TPCK, were added to the mixtures of D. suzukii testes and teratocytes. The status of the host tissues were recorded after 0 hr, and 30 hr …
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Figure 4—figure supplement 4—source data 1
Related to Figure 4—figure supplement 4C.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig4-figsupp4-data1-v1.xlsx
Figure 4—figure supplement 5
Inhibition of trypsins impairs the development of wasp larvae.
The length of the Td larvae in CK (H2O) and TLCK-injected hosts after 96 hr and 144 hr parasitization. Left to right: n=25, 24, 28, and 30 biologically independent larvae. Data represent the mean ± …
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Figure 4—figure supplement 5—source data 1
Related to Figure 4—figure supplement 5.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig4-figsupp5-data1-v1.xlsx
Figure 5 with 2 supplements
Superparasitism enhances Trichopria drosophilae (Td) parasitic efficiency.
(A) and (B) Parasitism rates (A) and wasp emergence rates (B) in 1- to 4-day-old D. suzukii pupae after monoparasitism or superparasitism by Td. Six biological replicates were performed. Data …
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Figure 5—source data 1
Related to Figure 5A.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-data1-v1.xlsx
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Figure 5—source data 2
Related to Figure 5B.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-data2-v1.xlsx
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Figure 5—source data 3
Related to Figure 5C.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-data3-v1.xlsx
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Figure 5—source data 4
Related to Figure 5D.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-data4-v1.xlsx
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Figure 5—source data 5
Related to Figure 5E.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-data5-v1.xlsx
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Figure 5—source data 6
Related to Figure 5G.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-data6-v1.xlsx
Figure 5—figure supplement 1
Superparasitism enhances Trichopria drosophilae (Td) parasitic efficiency on D. melanogaster.
(A) and (B) Parasitism rates (A) and wasp emergence rates (B) in 1- to 4-day-old D. melanogaster pupae after monoparasitism or superparasitism by Td. Six biological replicates were performed. Data …
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Figure 5—figure supplement 1—source data 1
Related to Figure 5—figure supplement 1A.
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Figure 5—figure supplement 1—source data 2
Related to Figure 5—figure supplement 1B.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-figsupp1-data2-v1.xlsx
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Figure 5—figure supplement 1—source data 3
Related to Figure 5—figure supplement 1C.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-figsupp1-data3-v1.xlsx
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Figure 5—figure supplement 1—source data 4
Related to Figure 5—figure supplement 1D.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-figsupp1-data4-v1.xlsx
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Figure 5—figure supplement 1—source data 5
Related to Figure 5—figure supplement 1E.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-figsupp1-data5-v1.xlsx
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Figure 5—figure supplement 1—source data 6
Related to Figure 5—figure supplement 1F.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig5-figsupp1-data6-v1.xlsx
Figure 5—figure supplement 2
The image of the host parasitized by two Trichopria drosophilae (Td) female wasps.
Two Td female wasps showed a collaboration to parasitize the same D. suzukii pupa. Scale bar: 500 μm.
Figure 6 with 1 supplement
Trichopria drosophilae (Td) avoids interspecific competition through chemoreception in the ovipositor.
(A) Schematic diagram of the Td interspecific competition assay. PH, Aj-parasitized host; NH, non-parasitized host. (B) Oviposition rates of Td in NH and PH pupae of D. suzukii and D. melanogaster, …
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Figure 6—source data 1
Related to Figure 6B.
- https://cdn.elifesciences.org/articles/94748/elife-94748-fig6-data1-v1.xlsx
Figure 6—figure supplement 1
Transcriptome expression profile of Orco on female antenna and ovipositor of Trichopria drosophilae (Td).
Figure 7
Genomic distribution and expression profiling of gustatory receptor genes in Trichopria drosophilae (Td).
(A) Genomic location of characterized gustatory receptor (GR) genes on Td chromosomes. (B) Transcriptome expression profiles of GR genes across representative tissues. The phylogeny is based on the …
Figure 8
Proposed model of the molecular and ecological adaptions underlying the parasitic success in Trichopria drosophilae (Td).
Td is a solitary parasitoid that presents high levels of pupal parasitism to Drosophila species, including D. suzukii. Td allows intraspecific superparatism to increase the success of wasp emergence …
Additional files
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Supplementary file 1
Basic features of Trichopria drosophilae genome.
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp1-v1.xlsx
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Supplementary file 2
Top 20 expanded gene families in Trichopria drosophilae (Td).
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp2-v1.xlsx
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Supplementary file 3
List of Trichopria drosophilae (Td) venom protein genes.
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp3-v1.xlsx
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Supplementary file 4
List of Trichopria drosophilae (Td) teratocyte genes.
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp4-v1.xlsx
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Supplementary file 5
List of Trichopria drosophilae (Td) chemoreception genes.
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp5-v1.xlsx
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Supplementary file 6
Primer sequences in this study.
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp6-v1.xlsx
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Supplementary file 7
Transcriptome sequencing data in this study.
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp7-v1.xlsx
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Supplementary file 8
Raw data in Figure 1—figure supplement 1D.
- https://cdn.elifesciences.org/articles/94748/elife-94748-supp8-v1.xlsx
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MDAR checklist
- https://cdn.elifesciences.org/articles/94748/elife-94748-mdarchecklist1-v1.docx
