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Sex and Death: Identification of Feedback Neuromodulation Balancing Reproduction and Survival

Neuroscience Bulletin volume 36, pages 1429–1440 (2020)Cite this article

Abstract

Some semelparous organisms in nature mate as many times as they can in a single reproductive episode before death, while most iteroparous species including humans avoid such suicidal reproductive behavior. Animals naturally pursue more sex and the possible fatal consequence of excessive sex must be orchestrated by negative feedback signals in iteroparous species, yet very little is known about the regulatory mechanisms. Here we used Drosophila male sexual behavior as a model system to study how excessive sex may kill males and how the nervous system reacts to prevent death by sex. We found that continuous sexual activity by activating the fruitless-expressing neurons induced a fixed multi-step behavioral pattern ending with male death. We further found negative feedback in the fly brain to prevent suicidal sexual behavior by expression changes of the neurotransmitters acetylcholine and gamma-aminobutyric acid, and neuropeptide F. These findings are crucial to understand the molecular underpinnings of how different organisms choose reproductive strategies and balance reproduction and survival.

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Acknowledgements

We thank the Tsinghua Fly Center and Bloomington Stock Center for the fly stocks. This work was supported by grants from the National Key R&D Program of China (2019YFA0802400), the National Natural Science Foundation of China (31970943, 31622028, and 31700920), and the Jiangsu Innovation and Entrepreneurship Team Program.

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Author notes

  1. Can Gao and Chao Guo are contributed equally to this work.

Affiliations

  1. The Key Laboratory of Developmental Genes and Human Disease, School of Life Science and Technology, Southeast University, Nanjing, 210096, China

    Can Gao, Qionglin Peng, Jie Cao & Yufeng Pan

  2. School of Life Sciences, Nantong University, Nantong, 226019, China

    Chao Guo & Dong Liu

  3. The Mina & Everard Goodman Faculty of Life Sciences and Susan Gonda Multidisciplinary Brain Research Center, Bar-Ilan University, Ramat-Gan, 5290002, Israel

    Galit Shohat-Ophir

  4. Co-innovation Center of Neuroregeneration, Nantong University, Nantong, 226019, China

    Dong Liu & Yufeng Pan

Authors
  1. Can Gao
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  2. Chao Guo
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  3. Qionglin Peng
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  4. Jie Cao
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  5. Galit Shohat-Ophir
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  6. Dong Liu
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  7. Yufeng Pan
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Correspondence to Yufeng Pan.

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Gao, C., Guo, C., Peng, Q. et al. Sex and Death: Identification of Feedback Neuromodulation Balancing Reproduction and Survival. Neurosci. Bull. 36, 1429–1440 (2020). https://doi.org/10.1007/s12264-020-00604-5

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  • DOI: https://doi.org/10.1007/s12264-020-00604-5

Keywords

  • Drosophila
  • Reproduction
  • Survival
  • NPF
  • GABA
  • Acetylcholine