IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32203-5.html
   My bibliography  Save this article

Search performance and octopamine neuronal signaling mediate parasitoid induced changes in Drosophila oviposition behavior

Author

Listed:
  • Lan Pang

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Zhiguo Liu

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Jiani Chen

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Zhi Dong

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Sicong Zhou

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Qichao Zhang

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Yueqi Lu

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Yifeng Sheng

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Xuexin Chen

    (Zhejiang University
    Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Jianhua Huang

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

Abstract

Making the appropriate responses to predation risk is essential for the survival of an organism; however, the underlying mechanisms are still largely unknown. Here, we find that Drosophila has evolved an adaptive strategy to manage the threat from its parasitoid wasp by manipulating the oviposition behavior. Through perception of the differences in host search performance of wasps, Drosophila is able to recognize younger wasps as a higher level of threat and consequently depress the oviposition. We further show that this antiparasitoid behavior is mediated by the regulation of the expression of Tdc2 and Tβh in the ventral nerve cord via LC4 visual projection neurons, which in turn leads to the dramatic reduction in octopamine and the resulting dysfunction of mature follicle trimming and rupture. Our study uncovers a detailed mechanism underlying the defensive behavior in insects that may advance our understanding of predator avoidance in animals.

Suggested Citation

  • Lan Pang & Zhiguo Liu & Jiani Chen & Zhi Dong & Sicong Zhou & Qichao Zhang & Yueqi Lu & Yifeng Sheng & Xuexin Chen & Jianhua Huang, 2022. "Search performance and octopamine neuronal signaling mediate parasitoid induced changes in Drosophila oviposition behavior," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32203-5
    DOI: 10.1038/s41467-022-32203-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32203-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-32203-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Pengfei Wei & Nan Liu & Zhijian Zhang & Xuemei Liu & Yongqiang Tang & Xiaobin He & Bifeng Wu & Zheng Zhou & Yaohan Liu & Juan Li & Yi Zhang & Xuanyi Zhou & Lin Xu & Lin Chen & Guoqiang Bi & Xintian Hu, 2015. "Correction: Corrigendum: Processing of visually evoked innate fear by a non-canonical thalamic pathway," Nature Communications, Nature, vol. 6(1), pages 1-1, November.
    2. Zheng Liu & Maro J. Kariya & Christopher D. Chute & Amy K. Pribadi & Sarah G. Leinwand & Ada Tong & Kevin P. Curran & Neelanjan Bose & Frank C. Schroeder & Jagan Srinivasan & Sreekanth H. Chalasani, 2018. "Predator-secreted sulfolipids induce defensive responses in C. elegans," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Jinho Jhang & Hyoeun Lee & Min Soo Kang & Han-Sol Lee & Hyungju Park & Jin-Hee Han, 2018. "Anterior cingulate cortex and its input to the basolateral amygdala control innate fear response," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    4. Fleur Ponton & Camille Lebarbenchon & Thierry Lefèvre & David G. Biron & David Duneau & David P. Hughes & Frédéric Thomas, 2006. "Parasite survives predation on its host," Nature, Nature, vol. 440(7085), pages 756-756, April.
    5. Zhiguo Ma & Tobias Stork & Dwight E. Bergles & Marc R. Freeman, 2016. "Neuromodulators signal through astrocytes to alter neural circuit activity and behaviour," Nature, Nature, vol. 539(7629), pages 428-432, November.
    6. Benjamin J. Ashton & Patrick Kennedy & Andrew N. Radford, 2020. "Interactions with conspecific outsiders as drivers of cognitive evolution," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    7. Zhu A. Wang & Jianhua Huang & Daniel Kalderon, 2012. "Drosophila follicle stem cells are regulated by proliferation and niche adhesion as well as mitochondria and ROS," Nature Communications, Nature, vol. 3(1), pages 1-10, January.
    8. Benjamin J. Ashton & Patrick Kennedy & Andrew N. Radford, 2020. "Author Correction: Interactions with conspecific outsiders as drivers of cognitive evolution," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    9. Jiani Chen & Gangqi Fang & Lan Pang & Yifeng Sheng & Qichao Zhang & Yuenan Zhou & Sicong Zhou & Yueqi Lu & Zhiguo Liu & Yixiang Zhang & Guiyun Li & Min Shi & Xuexin Chen & Shuai Zhan & Jianhua Huang, 2021. "Neofunctionalization of an ancient domain allows parasites to avoid intraspecific competition by manipulating host behaviour," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    10. Pengfei Wei & Nan Liu & Zhijian Zhang & Xuemei Liu & Yongqiang Tang & Xiaobin He & Bifeng Wu & Zheng Zhou & Yaohan Liu & Juan Li & Yi Zhang & Xuanyi Zhou & Lin Xu & Lin Chen & Guoqiang Bi & Xintian Hu, 2015. "Processing of visually evoked innate fear by a non-canonical thalamic pathway," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    11. Jianhua Huang & Jiani Chen & Gangqi Fang & Lan Pang & Sicong Zhou & Yuenan Zhou & Zhongqiu Pan & Qichao Zhang & Yifeng Sheng & Yueqi Lu & Zhiguo Liu & Yixiang Zhang & Guiyun Li & Min Shi & Xuexin Chen, 2021. "Two novel venom proteins underlie divergent parasitic strategies between a generalist and a specialist parasite," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    12. Congping Shang & Zijun Chen & Aixue Liu & Yang Li & Jiajing Zhang & Baole Qu & Fei Yan & Yaning Zhang & Weixiu Liu & Zhihui Liu & Xiaofei Guo & Dapeng Li & Yi Wang & Peng Cao, 2018. "Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    13. Shimaa A. M. Ebrahim & Gaëlle J. S. Talross & John R. Carlson, 2021. "Sight of parasitoid wasps accelerates sexual behavior and upregulates a micropeptide gene in Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    14. Fumika N. Hamada & Mark Rosenzweig & Kyeongjin Kang & Stefan R. Pulver & Alfredo Ghezzi & Timothy J. Jegla & Paul A. Garrity, 2008. "An internal thermal sensor controlling temperature preference in Drosophila," Nature, Nature, vol. 454(7201), pages 217-220, July.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Wei Shang & Shuangyi Xie & Wenbo Feng & Zhuangzhuang Li & Jingyan Jia & Xiaoxiao Cao & Yanting Shen & Jing Li & Haibo Shi & Yiran Gu & Shi-Jun Weng & Longnian Lin & Yi-Hsuan Pan & Xiao-Bing Yuan, 2024. "A non-image-forming visual circuit mediates the innate fear of heights in male mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Peñaherrera-Aguirre, Mateo & Sarraf, Matthew A. & Woodley of Menie, Michael A. & Miller, Geoffrey F., 2023. "The ten-million-year explosion: Paleocognitive reconstructions of domain-general cognitive ability (G) in extinct primates," Intelligence, Elsevier, vol. 101(C).
    3. Wen Z. Yang & Hengchang Xie & Xiaosa Du & Qian Zhou & Yan Xiao & Zhengdong Zhao & Xiaoning Jia & Jianhui Xu & Wen Zhang & Shuang Cai & Zhangjie Li & Xin Fu & Rong Hua & Junhao Cai & Shuang Chang & Jin, 2023. "A parabrachial-hypothalamic parallel circuit governs cold defense in mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. In-Jee You & Yeeun Bae & Alec R. Beck & Sora Shin, 2023. "Lateral hypothalamic proenkephalin neurons drive threat-induced overeating associated with a negative emotional state," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Junjun Gao & Song Zhang & Pan Deng & Zhigang Wu & Bruno Lemaitre & Zongzhao Zhai & Zheng Guo, 2024. "Dietary L-Glu sensing by enteroendocrine cells adjusts food intake via modulating gut PYY/NPF secretion," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    6. Allen P. F. Chen & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Shaoyu Ge & Qiaojie Xiong, 2023. "Nigrostriatal dopamine modulates the striatal-amygdala pathway in auditory fear conditioning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Nicole Pogodalla & Holger Kranenburg & Simone Rey & Silke Rodrigues & Albert Cardona & Christian Klämbt, 2021. "Drosophila ßHeavy-Spectrin is required in polarized ensheathing glia that form a diffusion-barrier around the neuropil," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    8. Huiling Yu & Liping Chen & Huiyang Lei & Guilin Pi & Rui Xiong & Tao Jiang & Dongqin Wu & Fei Sun & Yang Gao & Yuanhao Li & Wenju Peng & Bingyu Huang & Guoda Song & Xin Wang & Jingru Lv & Zetao Jin & , 2022. "Infralimbic medial prefrontal cortex signalling to calbindin 1 positive neurons in posterior basolateral amygdala suppresses anxiety- and depression-like behaviours," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Ami Ritter & Shlomi Habusha & Lior Givon & Shahaf Edut & Oded Klavir, 2024. "Prefrontal control of superior colliculus modulates innate escape behavior following adversity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Ke Yang & Yanghao Wang & Pek Jun Tiw & Chaoming Wang & Xiaolong Zou & Rui Yuan & Chang Liu & Ge Li & Chen Ge & Si Wu & Teng Zhang & Ru Huang & Yuchao Yang, 2024. "High-order sensory processing nanocircuit based on coupled VO2 oscillators," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    11. Valentina Botero & Bethany A. Stanhope & Elizabeth B. Brown & Eliza C. Grenci & Tamara Boto & Scarlet J. Park & Lanikea B. King & Keith R. Murphy & Kenneth J. Colodner & James A. Walker & Alex C. Keen, 2021. "Neurofibromin regulates metabolic rate via neuronal mechanisms in Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    12. Fushun Wang & Wei Wang & Simeng Gu & Dan Qi & Nathan A. Smith & Weiguo Peng & Wei Dong & Jiajin Yuan & Binbin Zhao & Ying Mao & Peng Cao & Qing Richard Lu & Lee A. Shapiro & S. Stephen Yi & Erxi Wu & , 2023. "Distinct astrocytic modulatory roles in sensory transmission during sleep, wakefulness, and arousal states in freely moving mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    13. Chen Zhang & Anmo J. Kim & Crisalesandra Rivera-Perez & Fernando G. Noriega & Young-Joon Kim, 2022. "The insect somatostatin pathway gates vitellogenesis progression during reproductive maturation and the post-mating response," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Kit D. Longden & Edward M. Rogers & Aljoscha Nern & Heather Dionne & Michael B. Reiser, 2023. "Different spectral sensitivities of ON- and OFF-motion pathways enhance the detection of approaching color objects in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    15. Yajie Liang & Rongwen Lu & Katharine Borges & Na Ji, 2023. "Stimulus edges induce orientation tuning in superior colliculus," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    16. Di Peng & Liubin Zheng & Dan Liu & Cheng Han & Xin Wang & Yan Yang & Li Song & Miaoying Zhao & Yanfeng Wei & Jiayi Li & Xiaoxue Ye & Yuxiang Wei & Zihao Feng & Xinhe Huang & Miaomiao Chen & Yujie Gou , 2024. "Large-language models facilitate discovery of the molecular signatures regulating sleep and activity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    17. Olga Kubrak & Takashi Koyama & Nadja Ahrentløv & Line Jensen & Alina Malita & Muhammad T. Naseem & Mette Lassen & Stanislav Nagy & Michael J. Texada & Kenneth V. Halberg & Kim Rewitz, 2022. "The gut hormone Allatostatin C/Somatostatin regulates food intake and metabolic homeostasis under nutrient stress," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32203-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.