Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila.
Drosophila larvae and pupae are at high risk of parasitoid infection in nature. To circumvent parasitic stress, fruit flies have developed various survival strategies, including cellular and behavioral defenses. We show that adult Drosophila females exposed to the parasitic wasps, Leptopilina boular...
Saved in:
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2021-03-01
|
| Series: | PLoS Genetics |
| Online Access: | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009456&type=printable |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850042417073356800 |
|---|---|
| author | Madhumala K Sadanandappa Shivaprasad H Sathyanarayana Shu Kondo Giovanni Bosco |
| author_facet | Madhumala K Sadanandappa Shivaprasad H Sathyanarayana Shu Kondo Giovanni Bosco |
| author_sort | Madhumala K Sadanandappa |
| collection | DOAJ |
| description | Drosophila larvae and pupae are at high risk of parasitoid infection in nature. To circumvent parasitic stress, fruit flies have developed various survival strategies, including cellular and behavioral defenses. We show that adult Drosophila females exposed to the parasitic wasps, Leptopilina boulardi, decrease their total egg-lay by deploying at least two strategies: Retention of fully developed follicles reduces the number of eggs laid, while induction of caspase-mediated apoptosis eliminates the vitellogenic follicles. These reproductive defense strategies require both visual and olfactory cues, but not the MB247-positive mushroom body neuronal function, suggesting a novel mode of sensory integration mediates reduced egg-laying in the presence of a parasitoid. We further show that neuropeptide F (NPF) signaling is necessary for both retaining matured follicles and activating apoptosis in vitellogenic follicles. Whereas previous studies have found that gut-derived NPF controls germ stem cell proliferation, we show that sensory-induced changes in germ cell development specifically require brain-derived NPF signaling, which recruits a subset of NPFR-expressing cell-types that control follicle development and retention. Importantly, we found that reduced egg-lay behavior is specific to parasitic wasps that infect the developing Drosophila larvae, but not the pupae. Our findings demonstrate that female fruit flies use multimodal sensory integration and neuroendocrine signaling via NPF to engage in parasite-specific cellular and behavioral survival strategies. |
| format | Article |
| id | doaj-art-1a337bc11df94f0fa78b6c52cbced2ee |
| institution | DOAJ |
| issn | 1553-7390 1553-7404 |
| language | English |
| publishDate | 2021-03-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj-art-1a337bc11df94f0fa78b6c52cbced2ee2025-08-20T02:55:33ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-03-01173e100945610.1371/journal.pgen.1009456Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila.Madhumala K SadanandappaShivaprasad H SathyanarayanaShu KondoGiovanni BoscoDrosophila larvae and pupae are at high risk of parasitoid infection in nature. To circumvent parasitic stress, fruit flies have developed various survival strategies, including cellular and behavioral defenses. We show that adult Drosophila females exposed to the parasitic wasps, Leptopilina boulardi, decrease their total egg-lay by deploying at least two strategies: Retention of fully developed follicles reduces the number of eggs laid, while induction of caspase-mediated apoptosis eliminates the vitellogenic follicles. These reproductive defense strategies require both visual and olfactory cues, but not the MB247-positive mushroom body neuronal function, suggesting a novel mode of sensory integration mediates reduced egg-laying in the presence of a parasitoid. We further show that neuropeptide F (NPF) signaling is necessary for both retaining matured follicles and activating apoptosis in vitellogenic follicles. Whereas previous studies have found that gut-derived NPF controls germ stem cell proliferation, we show that sensory-induced changes in germ cell development specifically require brain-derived NPF signaling, which recruits a subset of NPFR-expressing cell-types that control follicle development and retention. Importantly, we found that reduced egg-lay behavior is specific to parasitic wasps that infect the developing Drosophila larvae, but not the pupae. Our findings demonstrate that female fruit flies use multimodal sensory integration and neuroendocrine signaling via NPF to engage in parasite-specific cellular and behavioral survival strategies.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009456&type=printable |
| spellingShingle | Madhumala K Sadanandappa Shivaprasad H Sathyanarayana Shu Kondo Giovanni Bosco Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila. PLoS Genetics |
| title | Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila. |
| title_full | Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila. |
| title_fullStr | Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila. |
| title_full_unstemmed | Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila. |
| title_short | Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila. |
| title_sort | neuropeptide f signaling regulates parasitoid specific germline development and egg laying in drosophila |
| url | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009456&type=printable |
| work_keys_str_mv | AT madhumalaksadanandappa neuropeptidefsignalingregulatesparasitoidspecificgermlinedevelopmentandegglayingindrosophila AT shivaprasadhsathyanarayana neuropeptidefsignalingregulatesparasitoidspecificgermlinedevelopmentandegglayingindrosophila AT shukondo neuropeptidefsignalingregulatesparasitoidspecificgermlinedevelopmentandegglayingindrosophila AT giovannibosco neuropeptidefsignalingregulatesparasitoidspecificgermlinedevelopmentandegglayingindrosophila |