Resistance to natural and synthetic gene drive systems

Tom A R Price¹, Nikolai Windbichler², Robert L Unckless³, Andreas Sutter⁴, Jan-Niklas Runge⁵, Perran A Ross⁶, Andrew Pomiankowski⁷, Nicole L Nuckolls⁸, Catherine Montchamp-Moreau⁹, Nicole Mideo¹⁰, Oliver Y Martin¹¹, Andri Manser¹, Mathieu Legros^{12

13}, Amanda M Larracuente¹⁴, Luke Holman¹⁵, John Godwin¹⁶, Neil Gemmell¹⁷, Cécile Courret^{9

13}, Anna Buchman^{18

19}, Luke G Barrett¹², Anna K Lindholm⁵

Affiliations

¹ Department of Ecology, Evolution and Behaviour, University of Liverpool, Liverpool, UK.
² Department of Life Sciences, Imperial College London, London, UK.
³ Department of Molecular Biosciences, University of Kansas, Lawrence, KS, USA.
⁴ School of Biological Sciences, University of East Anglia, Norwich, UK.
⁵ Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.
⁶ Bio21 and the School of Biosciences, The University of Melbourne, Parkville, Victoria, Australia.
⁷ Department of Genetics, Evolution and Environment, University College London, London, UK.
⁸ Stowers Institute for Medical Research, Kansas City, MO, USA.
⁹ UMR Evolution Génome Comportement et Ecologie, Université Paris-Saclay, CNRS, IRD, Gif sur Yvette, France.
¹⁰ Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
¹¹ Department of Biology (D-BIOL) & Institute of Integrative Biology (IBZ), ETH Zurich, Zurich, Switzerland.
¹² CSIRO Agriculture and Food, Canberra, ACT, Australia.
¹³ CSIRO Synthetic Biology Future Science Platform, Canberra, ACT, Australia.
¹⁴ Department of Biology, University of Rochester, Rochester, NY, USA.
¹⁵ School of Biosciences, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁶ Department of Biological Sciences, North Carolina State University, Raleigh, NC, USA.
¹⁷ Department of Anatomy, University of Otago, Dunedin, New Zealand.
¹⁸ University of California, La Jolla, CA, USA.
¹⁹ Verily Life Sciences, South San Francisco, CA, USA.

PMID: 32969551
PMCID: PMC7796552
DOI: 10.1111/jeb.13693

Review

Resistance to natural and synthetic gene drive systems

Tom A R Price et al. J Evol Biol. 2020 Oct.

. 2020 Oct;33(10):1345-1360.

doi: 10.1111/jeb.13693. Epub 2020 Sep 24.

Authors

Affiliations

¹ Department of Ecology, Evolution and Behaviour, University of Liverpool, Liverpool, UK.
² Department of Life Sciences, Imperial College London, London, UK.
³ Department of Molecular Biosciences, University of Kansas, Lawrence, KS, USA.
⁴ School of Biological Sciences, University of East Anglia, Norwich, UK.
⁵ Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.
⁶ Bio21 and the School of Biosciences, The University of Melbourne, Parkville, Victoria, Australia.
⁷ Department of Genetics, Evolution and Environment, University College London, London, UK.
⁸ Stowers Institute for Medical Research, Kansas City, MO, USA.
⁹ UMR Evolution Génome Comportement et Ecologie, Université Paris-Saclay, CNRS, IRD, Gif sur Yvette, France.
¹⁰ Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
¹¹ Department of Biology (D-BIOL) & Institute of Integrative Biology (IBZ), ETH Zurich, Zurich, Switzerland.
¹² CSIRO Agriculture and Food, Canberra, ACT, Australia.
¹³ CSIRO Synthetic Biology Future Science Platform, Canberra, ACT, Australia.
¹⁴ Department of Biology, University of Rochester, Rochester, NY, USA.
¹⁵ School of Biosciences, The University of Melbourne, Melbourne, Victoria, Australia.
¹⁶ Department of Biological Sciences, North Carolina State University, Raleigh, NC, USA.
¹⁷ Department of Anatomy, University of Otago, Dunedin, New Zealand.
¹⁸ University of California, La Jolla, CA, USA.
¹⁹ Verily Life Sciences, South San Francisco, CA, USA.

PMID: 32969551
PMCID: PMC7796552
DOI: 10.1111/jeb.13693

Abstract

Scientists are rapidly developing synthetic gene drive elements intended for release into natural populations. These are intended to control or eradicate disease vectors and pests, or to spread useful traits through wild populations for disease control or conservation purposes. However, a crucial problem for gene drives is the evolution of resistance against them, preventing their spread. Understanding the mechanisms by which populations might evolve resistance is essential for engineering effective gene drive systems. This review summarizes our current knowledge of drive resistance in both natural and synthetic gene drives. We explore how insights from naturally occurring and synthetic drive systems can be integrated to improve the design of gene drives, better predict the outcome of releases and understand genomic conflict in general.

Keywords: Wolbachia; CRISPR-Cas9; fitness costs; meiotic drive; population suppression; selfish genetic elements; sex ratio distorter; transposable element.

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Conflict of interest statement

Conflicts of Interest Statement

The authors state they have no conflicts of interest to declare.

Figures

**Figure 1.**
The evolutionary impact of a gene drive, as measured by the magnitude and location of costs imposed (yellow/red gradients). Boxes represent individuals, white rectangles are chromosomes within the organism. Drive creates selection pressure for the three drive resistance mechanisms discussed in this review (blue). The selection pressure for drive resistance is highest at the target locus itself (1a), where rivalling homologous genes suffer both from reduced transmission due to drive (yellow) and (potential) fitness costs to the organism (red). Selection pressure on unlinked loci throughout the genome to disrupt drive will be a function of organismal drive costs (1b). Finally, gene drive may create selection for mechanisms that suppress the drive at the population level (2).

See this image and copyright information in PMC

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Resistance to natural and synthetic gene drive systems

Affiliations

Resistance to natural and synthetic gene drive systems

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources