Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts
Reproductive synchrony generally occurs in various group-living animals. However, the underlying mechanisms remain largely unexplored. The migratory locust, Locusta migratoria, a worldwide agricultural pest species, displays synchronous maturation and oviposition when forms huge swarm. The reproduct...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/74581 |
| _version_ | 1797998466177171456 |
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| author | Dafeng Chen Li Hou Jianing Wei Siyuan Guo Weichan Cui Pengcheng Yang Le Kang Xianhui Wang |
| author_facet | Dafeng Chen Li Hou Jianing Wei Siyuan Guo Weichan Cui Pengcheng Yang Le Kang Xianhui Wang |
| author_sort | Dafeng Chen |
| collection | DOAJ |
| description | Reproductive synchrony generally occurs in various group-living animals. However, the underlying mechanisms remain largely unexplored. The migratory locust, Locusta migratoria, a worldwide agricultural pest species, displays synchronous maturation and oviposition when forms huge swarm. The reproductive synchrony among group members is critical for the maintenance of locust swarms and population density of next generation. Here, we showed that gregarious female locusts displayed more synchronous sexual maturation and oviposition than solitarious females and olfactory deficiency mutants. Only the presence of gregarious male adults can stimulate sexual maturation synchrony of female adults. Of the volatiles emitted abundantly by gregarious male adults, the aggregation pheromone, 4-vinylanisole, was identified to play key role in inducing female sexual maturation synchrony. This maturation-accelerating effect of 4-vinylanisole disappeared in the females of Or35-/- lines, the mutants of 4-vinylanisole receptor. Interestingly, 4-vinylanisole displayed a time window action by which mainly accelerates oocyte maturation of young females aged at middle developmental stages (3–4 days post adult eclosion). We further revealed that juvenile hormone/vitellogenin pathway mediated female sexual maturation triggered by 4-vinylanisole. Our results highlight a ‘catch-up’ strategy by which gregarious females synchronize their oocyte maturation and oviposition by time-dependent endocrinal response to 4-vinylanisole, and provide insight into reproductive synchrony induced by olfactory signal released by heterosexual conspecifics in a given group. |
| first_indexed | 2024-04-11T10:49:10Z |
| format | Article |
| id | doaj.art-c0231087a0b946239394c2cdde86b0ac |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:49:10Z |
| publishDate | 2022-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-c0231087a0b946239394c2cdde86b0ac2022-12-22T04:28:58ZengeLife Sciences Publications LtdeLife2050-084X2022-03-011110.7554/eLife.74581Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locustsDafeng Chen0Li Hou1https://orcid.org/0000-0001-6727-7053Jianing Wei2Siyuan Guo3Weichan Cui4Pengcheng Yang5Le Kang6https://orcid.org/0000-0003-4262-2329Xianhui Wang7https://orcid.org/0000-0002-8732-829XState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, ChinaBeijing Institutes of Life Sciences, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China; Beijing Institutes of Life Sciences, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, ChinaReproductive synchrony generally occurs in various group-living animals. However, the underlying mechanisms remain largely unexplored. The migratory locust, Locusta migratoria, a worldwide agricultural pest species, displays synchronous maturation and oviposition when forms huge swarm. The reproductive synchrony among group members is critical for the maintenance of locust swarms and population density of next generation. Here, we showed that gregarious female locusts displayed more synchronous sexual maturation and oviposition than solitarious females and olfactory deficiency mutants. Only the presence of gregarious male adults can stimulate sexual maturation synchrony of female adults. Of the volatiles emitted abundantly by gregarious male adults, the aggregation pheromone, 4-vinylanisole, was identified to play key role in inducing female sexual maturation synchrony. This maturation-accelerating effect of 4-vinylanisole disappeared in the females of Or35-/- lines, the mutants of 4-vinylanisole receptor. Interestingly, 4-vinylanisole displayed a time window action by which mainly accelerates oocyte maturation of young females aged at middle developmental stages (3–4 days post adult eclosion). We further revealed that juvenile hormone/vitellogenin pathway mediated female sexual maturation triggered by 4-vinylanisole. Our results highlight a ‘catch-up’ strategy by which gregarious females synchronize their oocyte maturation and oviposition by time-dependent endocrinal response to 4-vinylanisole, and provide insight into reproductive synchrony induced by olfactory signal released by heterosexual conspecifics in a given group.https://elifesciences.org/articles/74581social interactionsexual maturationolfactory signalendocrine hormonepheromonessynchrony |
| spellingShingle | Dafeng Chen Li Hou Jianing Wei Siyuan Guo Weichan Cui Pengcheng Yang Le Kang Xianhui Wang Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts eLife social interaction sexual maturation olfactory signal endocrine hormone pheromones synchrony |
| title | Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts |
| title_full | Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts |
| title_fullStr | Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts |
| title_full_unstemmed | Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts |
| title_short | Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts |
| title_sort | aggregation pheromone 4 vinylanisole promotes the synchrony of sexual maturation in female locusts |
| topic | social interaction sexual maturation olfactory signal endocrine hormone pheromones synchrony |
| url | https://elifesciences.org/articles/74581 |
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