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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
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    References listed on IDEAS

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    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. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
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