IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-54369-w.html
   My bibliography  Save this article

Mating reconciles fitness and fecundity by switching diet preference in flies

Author

Listed:
  • Chenxi Liu

    (Tsinghua University
    Tsinghua University
    China Agricultural University)

  • Ning Tian

    (Tsinghua University
    Tsinghua University)

  • Pei Chang

    (Tsinghua University)

  • Wei Zhang

    (Tsinghua University
    Tsinghua University)

Abstract

Protein-rich diets shorten lifespan but increase fecundity in many organisms. Animals actively adjust their feeding behavior to meet their nutritional requirements. However, the neural mechanisms underlying the dynamic regulation of protein consumption remain unclear. Here we find that both sexes of fruit flies exhibit a preference for protein food before mating to prepare for reproduction. Mated female flies display an increased appetite for yeast to benefit their offspring, albeit at the cost of stress resistance and lifespan. In contrast, males show a momentarily reduced yeast appetite after mating likely to restore their fitness. This mating state-dependent switch between sexes is mediated by a sexually dimorphic neural circuit labeled with leucokinin in the anterior brain. Furthermore, intermittent yeast consumption benefits both the lifespan and fecundity of males, while maximizing female fecundity without compromising lifespan.

Suggested Citation

  • Chenxi Liu & Ning Tian & Pei Chang & Wei Zhang, 2024. "Mating reconciles fitness and fecundity by switching diet preference in flies," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54369-w
    DOI: 10.1038/s41467-024-54369-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-54369-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-54369-w?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. Boram Kim & Makoto I. Kanai & Yangkyun Oh & Minsoo Kyung & Eun-Kyoung Kim & In-Hwan Jang & Ji-Hoon Lee & Sang-Gyu Kim & Greg S. B. Suh & Won-Jae Lee, 2021. "Response of the microbiome–gut–brain axis in Drosophila to amino acid deficit," Nature, Nature, vol. 593(7860), pages 570-574, May.
    2. Jean-Christophe Billeter & Jade Atallah & Joshua J. Krupp & Jocelyn G. Millar & Joel D. Levine, 2009. "Specialized cells tag sexual and species identity in Drosophila melanogaster," Nature, Nature, vol. 461(7266), pages 987-991, October.
    3. Hui-Hao Lin & Meihua Christina Kuang & Imran Hossain & Yinan Xuan & Laura Beebe & Andrew K. Shepherd & Marco Rolandi & Jing W. Wang, 2022. "A nutrient-specific gut hormone arbitrates between courtship and feeding," Nature, Nature, vol. 602(7898), pages 632-638, February.
    4. Daniel Münch & Dennis Goldschmidt & Carlos Ribeiro, 2022. "The neuronal logic of how internal states control food choice," Nature, Nature, vol. 607(7920), pages 747-755, July.
    5. Elizabeth B Brown & Kreesha D Shah & Richard Faville & Benjamin Kottler & Alex C Keene, 2020. "Drosophila insulin-like peptide 2 mediates dietary regulation of sleep intensity," PLOS Genetics, Public Library of Science, vol. 16(3), pages 1-26, March.
    6. Fei Wang & Kaiyu Wang & Nora Forknall & Christopher Patrick & Tansy Yang & Ruchi Parekh & Davi Bock & Barry J. Dickson, 2020. "Neural circuitry linking mating and egg laying in Drosophila females," Nature, Nature, vol. 579(7797), pages 101-105, March.
    7. Richard C. Grandison & Matthew D. W. Piper & Linda Partridge, 2009. "Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila," Nature, Nature, vol. 462(7276), pages 1061-1064, December.
    8. Pavel M. Itskov & José-Maria Moreira & Ekaterina Vinnik & Gonçalo Lopes & Steve Safarik & Michael H. Dickinson & Carlos Ribeiro, 2014. "Automated monitoring and quantitative analysis of feeding behaviour in Drosophila," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    9. Maria E Yurgel & Priyanka Kakad & Meet Zandawala & Dick R Nässel & Tanja A Godenschwege & Alex C Keene, 2019. "A single pair of leucokinin neurons are modulated by feeding state and regulate sleep–metabolism interactions," PLOS Biology, Public Library of Science, vol. 17(2), pages 1-26, February.
    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. 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.
    2. Raquel Álvarez-Ocaña & Michael P. Shahandeh & Vijayaditya Ray & Thomas O. Auer & Nicolas Gompel & Richard Benton, 2023. "Odor-regulated oviposition behavior in an ecological specialist," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Ziwei Dai & Weiyan Zheng & Jason W. Locasale, 2022. "Amino acid variability, tradeoffs and optimality in human diet," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Cristal M. Hill & Diana C. Albarado & Lucia G. Coco & Redin A. Spann & Md Shahjalal Khan & Emily Qualls-Creekmore & David H. Burk & Susan J. Burke & J. Jason Collier & Sangho Yu & David H. McDougal & , 2022. "FGF21 is required for protein restriction to extend lifespan and improve metabolic health in male mice," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Tyler R. Sizemore & Julius Jonaitis & Andrew M. Dacks, 2023. "Heterogeneous receptor expression underlies non-uniform peptidergic modulation of olfaction in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    6. Noha Sharafeldin & Martha L. Slattery & Qi Liu & Conrado Franco-Villalobos & Bette J. Caan & John D. Potter & Yutaka Yasui, 2017. "Multiple Gene-Environment Interactions on the Angiogenesis Gene-Pathway Impact Rectal Cancer Risk and Survival," IJERPH, MDPI, vol. 14(10), pages 1-15, September.
    7. Hina Kosakamoto & Fumiaki Obata & Junpei Kuraishi & Hide Aikawa & Rina Okada & Joshua N. Johnstone & Taro Onuma & Matthew D. W. Piper & Masayuki Miura, 2023. "Early-adult methionine restriction reduces methionine sulfoxide and extends lifespan in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Evan S. Schaffer & Neeli Mishra & Matthew R. Whiteway & Wenze Li & Michelle B. Vancura & Jason Freedman & Kripa B. Patel & Venkatakaushik Voleti & Liam Paninski & Elizabeth M. C. Hillman & L. F. Abbot, 2023. "The spatial and temporal structure of neural activity across the fly brain," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Jin-Hyuck Jeong & Jun-Seok Han & Youngae Jung & Seung-Min Lee & So-Hyun Park & Mooncheol Park & Min-Gi Shin & Nami Kim & Mi Sun Kang & Seokho Kim & Kwang-Pyo Lee & Ki-Sun Kwon & Chun-A. Kim & Yong Ryo, 2023. "A new AMPK isoform mediates glucose-restriction induced longevity non-cell autonomously by promoting membrane fluidity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Elizabeth B Brown & Kreesha D Shah & Richard Faville & Benjamin Kottler & Alex C Keene, 2020. "Drosophila insulin-like peptide 2 mediates dietary regulation of sleep intensity," PLOS Genetics, Public Library of Science, vol. 16(3), pages 1-26, March.
    11. Mami Nakamizo-Dojo & Kenichi Ishii & Jiro Yoshino & Masato Tsuji & Kazuo Emoto, 2023. "Descending GABAergic pathway links brain sugar-sensing to peripheral nociceptive gating in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Rebecca Rooke & Joshua J. Krupp & Amara Rasool & Mireille Golemiec & Megan Stewart & Jonathan Schneider & Joel D. Levine, 2024. "The gene “degrees of kevin bacon” (dokb) regulates a social network behaviour in Drosophila melanogaster," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    13. Thomas A. Verschut & Renny Ng & Nicolas P. Doubovetzky & Guillaume Calvez & Jan L. Sneep & Adriaan J. Minnaard & Chih-Ying Su & Mikael A. Carlsson & Bregje Wertheim & Jean-Christophe Billeter, 2023. "Aggregation pheromones have a non-linear effect on oviposition behavior in Drosophila melanogaster," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. 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.
    15. Minhao Li & Dawn S. Chen & Ian P. Junker & Fabianna I. Szorenyi & Guan Hao Chen & Arnold J. Berger & Aaron A. Comeault & Daniel R. Matute & Yun Ding, 2024. "Ancestral neural circuits potentiate the origin of a female sexual behavior in Drosophila," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    16. Qiankun He & Juan Du & Liya Wei & Zhangwu Zhao, 2020. "AKH-FOXO pathway regulates starvation-induced sleep loss through remodeling of the small ventral lateral neuron dorsal projections," PLOS Genetics, Public Library of Science, vol. 16(10), pages 1-21, October.
    17. Shivesh Chaudhary & Sihoon Moon & Hang Lu, 2022. "Fast, efficient, and accurate neuro-imaging denoising via supervised deep learning," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Yunpo Zhao & Mohammed A. Khallaf & Emilia Johansson & Najat Dzaki & Shreelatha Bhat & Johannes Alfredsson & Jianli Duan & Bill S. Hansson & Markus Knaden & Mattias Alenius, 2022. "Hedgehog-mediated gut-taste neuron axis controls sweet perception in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    19. Grace Y. Liu & Patrick Jouandin & Raymond E. Bahng & Norbert Perrimon & David M. Sabatini, 2024. "An evolutionary mechanism to assimilate new nutrient sensors into the mTORC1 pathway," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    20. Tatyana Y Fedina & Tsung-Han Kuo & Klaus Dreisewerd & Herman A Dierick & Joanne Y Yew & Scott D Pletcher, 2012. "Dietary Effects on Cuticular Hydrocarbons and Sexual Attractiveness in Drosophila," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-11, 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:15:y:2024:i:1:d:10.1038_s41467-024-54369-w. 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.