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Targeting mosquito X-chromosomes reveals complex transmission dynamics of sex ratio distorting gene drives

Author

Listed:
  • Daniella An Haber

    (Hebrew University of Jerusalem)

  • Yael Arien

    (Hebrew University of Jerusalem)

  • Lee Benjamin Lamdan

    (Hebrew University of Jerusalem)

  • Yehonathan Alcalay

    (Hebrew University of Jerusalem)

  • Chen Zecharia

    (Hebrew University of Jerusalem)

  • Flavia Krsticevic

    (Hebrew University of Jerusalem)

  • Elad Shmuel Yonah

    (Hebrew University of Jerusalem)

  • Rotem Daniel Avraham

    (Hebrew University of Jerusalem)

  • Elzbieta Krzywinska

    (The Pirbright Institute
    Alice Holt Lodge)

  • Jaroslaw Krzywinski

    (The Pirbright Institute
    Polo d’Innovazione di Genomica Genetica e Biologia, Via Mazzieri)

  • Eric Marois

    (Université de Strasbourg, INSERM, CNRS)

  • Nikolai Windbichler

    (Imperial College London)

  • Philippos Aris Papathanos

    (Hebrew University of Jerusalem)

Abstract

Engineered sex ratio distorters (SRDs) have been proposed as a powerful component of genetic control strategies designed to suppress harmful insect pests. Two types of CRISPR-based SRD mechanisms have been proposed: X-shredding, which eliminates X-bearing sperm, and X-poisoning, which eliminates females inheriting disrupted X-chromosomes. These differences can have a profound impact on the population dynamics of SRDs when linked to the Y-chromosome: an X-shredder is invasive, constituting a classical meiotic Y-drive, whereas X-poisoning is self-limiting, unable to invade but also insulated from selection. Here, we establish X-poisoning strains in the malaria vector Anopheles gambiae targeting three X-linked genes during spermatogenesis, resulting in male bias. We find that sex distortion is primarily driven by a loss of X-bearing sperm, with limited evidence for postzygotic lethality of female progeny. By leveraging a Drosophila melanogaster model, we show unambiguously that engineered SRD traits can operate differently in these two insects. Unlike X-shredding, X-poisoning could theoretically operate at early stages of spermatogenesis. We therefore explore premeiotic Cas9 expression to target the mosquito X-chromosome. We find that, by pre-empting the onset of meiotic sex chromosome inactivation, this approach may enable the development of Y-linked SRDs if mutagenesis of spermatogenesis-essential genes is functionally balanced.

Suggested Citation

  • Daniella An Haber & Yael Arien & Lee Benjamin Lamdan & Yehonathan Alcalay & Chen Zecharia & Flavia Krsticevic & Elad Shmuel Yonah & Rotem Daniel Avraham & Elzbieta Krzywinska & Jaroslaw Krzywinski & E, 2024. "Targeting mosquito X-chromosomes reveals complex transmission dynamics of sex ratio distorting gene drives," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49387-7
    DOI: 10.1038/s41467-024-49387-7
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    References listed on IDEAS

    as
    1. Andreas J. Berghammer & Martin Klingler & Ernst A. Wimmer, 1999. "A universal marker for transgenic insects," Nature, Nature, vol. 402(6760), pages 370-371, November.
    2. Roberto Galizi & Lindsey A. Doyle & Miriam Menichelli & Federica Bernardini & Anne Deredec & Austin Burt & Barry L. Stoddard & Nikolai Windbichler & Andrea Crisanti, 2014. "A synthetic sex ratio distortion system for the control of the human malaria mosquito," Nature Communications, Nature, vol. 5(1), pages 1-8, September.
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