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Engineered Reciprocal Chromosome Translocations Drive High Threshold, Reversible Population Replacement in Drosophila

  • Anna B. Buchman
    Anna B. Buchman
    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, United States
    Division of Biological Sciences, University of California, San Diego, California 92161, United States
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    Orcidhttp://orcid.org/0000-0002-8775-6147
    • , 
  • Tobin Ivy
    Tobin Ivy
    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, United States
    More by Tobin Ivy
    • , 
  • John M. Marshall
    John M. Marshall
    School of Public Health, University of California, Berkeley, California 94720, United States
    More by John M. Marshall
    • , 
  • Omar S. Akbari*
    Omar S. Akbari
    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, United States
    Division of Biological Sciences, University of California, San Diego, California 92161, United States
    *E-mail: [email protected]
    More by Omar S. Akbari
    Orcidhttp://orcid.org/0000-0002-6853-9884
    • , and 
  • Bruce A. Hay*
    Bruce A. Hay
    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, United States
    Division of Biological Sciences, University of California, San Diego, California 92161, United States
    *E-mail: [email protected]
    More by Bruce A. Hay
Cite this: ACS Synth. Biol. 2018, 7, 5, 1359–1370
Publication Date (Web):April 2, 2018
https://doi.org/10.1021/acssynbio.7b00451
Copyright © 2018 American Chemical Society
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Abstract

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Replacement of wild insect populations with transgene-bearing individuals unable to transmit disease or survive under specific environmental conditions using gene drive provides a self-perpetuating method of disease prevention. Mechanisms that require the gene drive element and linked cargo to exceed a high threshold frequency in order for spread to occur are attractive because they offer several points of control: they bring about local, but not global population replacement; and transgenes can be eliminated by reintroducing wildtypes into the population so as to drive the frequency of transgenes below the threshold frequency required for drive. Reciprocal chromosome translocations were proposed as a tool for bringing about high threshold population replacement in 1940 and 1968. However, translocations able to achieve this goal have only been reported once, in the spider mite Tetranychus urticae, a haplo-diploid species in which there is strong selection in haploid males for fit homozygotes. We report the creation of engineered translocation-bearing strains of Drosophila melanogaster, generated through targeted chromosomal breakage and homologous recombination. These strains drive high threshold population replacement in laboratory populations. While it remains to be shown that engineered translocations can bring about population replacement in wild populations, these observations suggest that further exploration of engineered translocations as a tool for controlled population replacement is warranted.

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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acssynbio.7b00451.

  • Supplementary Methods describing the general theoretical framework of the modeling used and the specifics and comparison of various investigated fitness cost models, as well as Supplementary Figure 1 and Supplementary Table 1 (PDF)

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Cited By

This article is cited by 15 publications.

  1. Jackson Champer, Joanna Zhao, Samuel E. Champer, Jingxian Liu, Philipp W. Messer. Population Dynamics of Underdominance Gene Drive Systems in Continuous Space. ACS Synthetic Biology 2020, 9 (4) , 779-792. https://doi.org/10.1021/acssynbio.9b00452
  2. Héctor M. Sánchez C., Jared B. Bennett, Sean L. Wu, Gordana Rašić, Omar S. Akbari, John M. Marshall. Modeling confinement and reversibility of threshold-dependent gene drive systems in spatially-explicit Aedes aegypti populations. BMC Biology 2020, 18 (1) https://doi.org/10.1186/s12915-020-0759-9
  3. Maciej Maselko, Nathan Feltman, Ambuj Upadhyay, Amanda Hayward, Siba Das, Nathan Myslicki, Aidan J. Peterson, Michael B. O’Connor, Michael J. Smanski. Engineering multiple species-like genetic incompatibilities in insects. Nature Communications 2020, 11 (1) https://doi.org/10.1038/s41467-020-18348-1
  4. Tom A. R. Price, Nikolai Windbichler, Robert L. Unckless, Andreas Sutter, Jan‐Niklas Runge, Perran A. Ross, Andrew Pomiankowski, Nicole L. Nuckolls, Catherine Montchamp‐Moreau, Nicole Mideo, Oliver Y. Martin, Andri Manser, Mathieu Legros, Amanda M. Larracuente, Luke Holman, John Godwin, Neil Gemmell, Cécile Courret, Anna Buchman, Luke G. Barrett, Anna K. Lindholm. Resistance to natural and synthetic gene drive systems. Journal of Evolutionary Biology 2020, 33 (10) , 1345-1360. https://doi.org/10.1111/jeb.13693
  5. Robyn R. Raban, Omar S. Akbari. A day in the life of a mosquito insectary team: pushing for solutions to mosquito-borne diseases. Lab Animal 2020, 49 (9) , 241-243. https://doi.org/10.1038/s41684-020-0617-y
  6. Georg Oberhofer, Tobin Ivy, Bruce A. Hay. Gene drive and resilience through renewal with next generation Cleave and Rescue selfish genetic elements. Proceedings of the National Academy of Sciences 2020, 14 , 201921698. https://doi.org/10.1073/pnas.1921698117
  7. Stephanie Gamez, Igor Antoshechkin, Stelia C. Mendez-Sanchez, Omar S. Akbari. The Developmental Transcriptome of Aedes albopictus , a Major Worldwide Human Disease Vector. G3: Genes|Genomes|Genetics 2020, 10 (3) , 1051-1062. https://doi.org/10.1534/g3.119.401006
  8. Robyn R. Raban, John M. Marshall, Omar S. Akbari. Progress towards engineering gene drives for population control. The Journal of Experimental Biology 2020, 223 (Suppl 1) , jeb208181. https://doi.org/10.1242/jeb.208181
  9. Nikolay P. Kandul, Junru Liu, Anna Buchman, Valentino M. Gantz, Ethan Bier, Omar S. Akbari. Assessment of a Split Homing Based Gene Drive for Efficient Knockout of Multiple Genes. G3: Genes|Genomes|Genetics 2020, 10 (2) , 827-837. https://doi.org/10.1534/g3.119.400985
  10. Héctor M. Sánchez C., Sean L. Wu, Jared B. Bennett, John M. Marshall, . MGD riv E: A modular simulation framework for the spread of gene drives through spatially explicit mosquito populations. Methods in Ecology and Evolution 2020, 11 (2) , 229-239. https://doi.org/10.1111/2041-210X.13318
  11. Gregory A Backus, Jason A Delborne. Threshold-Dependent Gene Drives in the Wild: Spread, Controllability, and Ecological Uncertainty. BioScience 2019, 69 (11) , 900-907. https://doi.org/10.1093/biosci/biz098
  12. Sumit Dhole, Alun L. Lloyd, Fred Gould. Tethered homing gene drives: A new design for spatially restricted population replacement and suppression. Evolutionary Applications 2019, 12 (8) , 1688-1702. https://doi.org/10.1111/eva.12827
  13. Dominique Brossard, Pam Belluck, Fred Gould, Christopher D. Wirz. Promises and perils of gene drives: Navigating the communication of complex, post-normal science. Proceedings of the National Academy of Sciences 2019, 116 (16) , 7692-7697. https://doi.org/10.1073/pnas.1805874115
  14. James J. Bull, Christopher H. Remien, Richard Gomulkiewicz, Stephen M. Krone. Spatial structure undermines parasite suppression by gene drive cargo. PeerJ 2019, 7 , e7921. https://doi.org/10.7717/peerj.7921
  15. Philip T. Leftwich, Matthew P. Edgington, Tim Harvey-Samuel, Leonela Z. Carabajal Paladino, Victoria C. Norman, Luke Alphey. Recent advances in threshold-dependent gene drives for mosquitoes. Biochemical Society Transactions 2018, 46 (5) , 1203-1212. https://doi.org/10.1042/BST20180076

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