IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48960-4.html
   My bibliography  Save this article

Rapid response of fly populations to gene dosage across development and generations

Author

Listed:
  • Xueying C. Li

    (European Molecular Biology Laboratory (EMBL)
    Beijing Normal University)

  • Lautaro Gandara

    (European Molecular Biology Laboratory (EMBL))

  • Måns Ekelöf

    (European Molecular Biology Laboratory (EMBL))

  • Kerstin Richter

    (European Molecular Biology Laboratory (EMBL))

  • Theodore Alexandrov

    (European Molecular Biology Laboratory (EMBL)
    Molecular Medicine Partnership Unit between EMBL and Heidelberg University
    BioInnovation Institute)

  • Justin Crocker

    (European Molecular Biology Laboratory (EMBL))

Abstract

Although the effects of genetic and environmental perturbations on multicellular organisms are rarely restricted to single phenotypic layers, our current understanding of how developmental programs react to these challenges remains limited. Here, we have examined the phenotypic consequences of disturbing the bicoid regulatory network in early Drosophila embryos. We generated flies with two extra copies of bicoid, which causes a posterior shift of the network’s regulatory outputs and a decrease in fitness. We subjected these flies to EMS mutagenesis, followed by experimental evolution. After only 8–15 generations, experimental populations have normalized patterns of gene expression and increased survival. Using a phenomics approach, we find that populations were normalized through rapid increases in embryo size driven by maternal changes in metabolism and ovariole development. We extend our results to additional populations of flies, demonstrating predictability. Together, our results necessitate a broader view of regulatory network evolution at the systems level.

Suggested Citation

  • Xueying C. Li & Lautaro Gandara & Måns Ekelöf & Kerstin Richter & Theodore Alexandrov & Justin Crocker, 2024. "Rapid response of fly populations to gene dosage across development and generations," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48960-4
    DOI: 10.1038/s41467-024-48960-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48960-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-48960-4?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. Feng He & Chuanxian Wei & Honggang Wu & David Cheung & Renjie Jiao & Jun Ma, 2015. "Fundamental origins and limits for scaling a maternal morphogen gradient," Nature Communications, Nature, vol. 6(1), pages 1-10, May.
    2. Benjamin H. Good & Michael J. McDonald & Jeffrey E. Barrick & Richard E. Lenski & Michael M. Desai, 2017. "The dynamics of molecular evolution over 60,000 generations," Nature, Nature, vol. 551(7678), pages 45-50, November.
    3. Nicolás Frankel & Deniz F. Erezyilmaz & Alistair P. McGregor & Shu Wang & François Payre & David L. Stern, 2011. "Morphological evolution caused by many subtle-effect substitutions in regulatory DNA," Nature, Nature, vol. 474(7353), pages 598-603, June.
    4. Samuel H. Church & Seth Donoughe & Bruno A. S. de Medeiros & Cassandra G. Extavour, 2019. "Insect egg size and shape evolve with ecology but not developmental rate," Nature, Nature, vol. 571(7763), pages 58-62, July.
    5. Bahram Houchmandzadeh & Eric Wieschaus & Stanislas Leibler, 2002. "Establishment of developmental precision and proportions in the early Drosophila embryo," Nature, Nature, vol. 415(6873), pages 798-802, February.
    6. Sasha F. Levy & Jamie R. Blundell & Sandeep Venkataram & Dmitri A. Petrov & Daniel S. Fisher & Gavin Sherlock, 2015. "Quantitative evolutionary dynamics using high-resolution lineage tracking," Nature, Nature, vol. 519(7542), pages 181-186, March.
    7. Timothy Fuqua & Jeff Jordan & Maria Elize Breugel & Aliaksandr Halavatyi & Christian Tischer & Peter Polidoro & Namiko Abe & Albert Tsai & Richard S. Mann & David L. Stern & Justin Crocker, 2020. "Dense and pleiotropic regulatory information in a developmental enhancer," Nature, Nature, vol. 587(7833), pages 235-239, November.
    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. Joao A. Ascensao & Kelly M. Wetmore & Benjamin H. Good & Adam P. Arkin & Oskar Hallatschek, 2023. "Quantifying the local adaptive landscape of a nascent bacterial community," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Yurie Okabe-Oho & Hiroki Murakami & Suguru Oho & Masaki Sasai, 2009. "Stable, Precise, and Reproducible Patterning of Bicoid and Hunchback Molecules in the Early Drosophila Embryo," PLOS Computational Biology, Public Library of Science, vol. 5(8), pages 1-20, August.
    3. Casper J Breuker & James S Patterson & Christian Peter Klingenberg, 2006. "A Single Basis for Developmental Buffering of Drosophila Wing Shape," PLOS ONE, Public Library of Science, vol. 1(1), pages 1-7, December.
    4. Seth Donoughe & Jordan Hoffmann & Taro Nakamura & Chris H. Rycroft & Cassandra G. Extavour, 2022. "Nuclear speed and cycle length co-vary with local density during syncytial blastoderm formation in a cricket," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Piaopiao Chen & Jianzhi Zhang, 2024. "The loci of environmental adaptation in a model eukaryote," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Serhii Aif & Nico Appold & Lucas Kampman & Oskar Hallatschek & Jona Kayser, 2022. "Evolutionary rescue of resistant mutants is governed by a balance between radial expansion and selection in compact populations," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Daniel P. G. H. Wong & Benjamin H. Good, 2024. "Quantifying the adaptive landscape of commensal gut bacteria using high-resolution lineage tracking," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Sébastien Boyer & Lucas Hérissant & Gavin Sherlock, 2021. "Adaptation is influenced by the complexity of environmental change during evolution in a dynamic environment," PLOS Genetics, Public Library of Science, vol. 17(1), pages 1-27, January.
    9. Avik Mukherjee & Jade Ealy & Yanqing Huang & Nina Catherine Benites & Mark Polk & Markus Basan, 2023. "Coexisting ecotypes in long-term evolution emerged from interacting trade-offs," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    10. N. Frazão & A. Konrad & M. Amicone & E. Seixas & D. Güleresi & M. Lässig & I. Gordo, 2022. "Two modes of evolution shape bacterial strain diversity in the mammalian gut for thousands of generations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Jingyuan Deng & Wei Wang & Long Jason Lu & Jun Ma, 2010. "A Two-Dimensional Simulation Model of the Bicoid Gradient in Drosophila," PLOS ONE, Public Library of Science, vol. 5(4), pages 1-11, April.
    12. Roman Vetter & Dagmar Iber, 2022. "Precision of morphogen gradients in neural tube development," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Francisco J P Lopes & Fernando M C Vieira & David M Holloway & Paulo M Bisch & Alexander V Spirov, 2008. "Spatial Bistability Generates hunchback Expression Sharpness in the Drosophila Embryo," PLOS Computational Biology, Public Library of Science, vol. 4(9), pages 1-14, September.
    14. Li Xie & Wenying Shou, 2021. "Steering ecological-evolutionary dynamics to improve artificial selection of microbial communities," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    15. Ryo Mizuuchi & Taro Furubayashi & Norikazu Ichihashi, 2022. "Evolutionary transition from a single RNA replicator to a multiple replicator network," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    16. Hadel Al Asafen & Prasad U Bandodkar & Sophia Carrell-Noel & Allison E Schloop & Jeramey Friedman & Gregory T Reeves, 2020. "Robustness of the Dorsal morphogen gradient with respect to morphogen dosage," PLOS Computational Biology, Public Library of Science, vol. 16(4), pages 1-21, April.
    17. Shawn C Little & Gašper Tkačik & Thomas B Kneeland & Eric F Wieschaus & Thomas Gregor, 2011. "The Formation of the Bicoid Morphogen Gradient Requires Protein Movement from Anteriorly Localized mRNA," PLOS Biology, Public Library of Science, vol. 9(3), pages 1-17, March.
    18. Joseph J. Hale & Takeshi Matsui & Ilan Goldstein & Martin N. Mullis & Kevin R. Roy & Christopher Ne Ville & Darach Miller & Charley Wang & Trevor Reynolds & Lars M. Steinmetz & Sasha F. Levy & Ian M. , 2024. "Genome-scale analysis of interactions between genetic perturbations and natural variation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Jeremy A. Owen & Jordan M. Horowitz, 2023. "Size limits the sensitivity of kinetic schemes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    20. Cauã Antunes Westmann & Leander Goldbach & Andreas Wagner, 2024. "The highly rugged yet navigable regulatory landscape of the bacterial transcription factor TetR," Nature Communications, Nature, vol. 15(1), pages 1-20, 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_s41467-024-48960-4. 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.