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Dodging silver bullets: good CRISPR gene-drive design is critical for eradicating exotic vertebrates

Thomas A. A. Prowse, Phillip Cassey, Joshua V. Ross, Chandran Pfitzner, Talia A. Wittmann, Paul Thomas
Published 9 August 2017.DOI: 10.1098/rspb.2017.0799
Thomas A. A. Prowse
School of Mathematical Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia
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  • For correspondence: thomas.prowse@adelaide.edu.au
Phillip Cassey
The Environment Institute and School of Biological Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia
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Joshua V. Ross
School of Mathematical Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia
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Chandran Pfitzner
The Environment Institute and School of Biological Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia
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Talia A. Wittmann
The Environment Institute and School of Biological Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia
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Paul Thomas
The Environment Institute and School of Biological Sciences, The University of Adelaide, Adelaide, South Australia 5005, AustraliaThe Robinson Research Institute, The University of Adelaide, Adelaide, South Australia 5005, Australia
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Abstract

Self-replicating gene drives that can spread deleterious alleles through animal populations have been promoted as a much needed but controversial ‘silver bullet’ for controlling invasive alien species. Homing-based drives comprise an endonuclease and a guide RNA (gRNA) that are replicated during meiosis via homologous recombination. However, their efficacy for controlling wild populations is threatened by inherent polymorphic resistance and the creation of resistance alleles via non-homologous end-joining (NHEJ)-mediated DNA repair. We used stochastic individual-based models to identify realistic gene-drive strategies capable of eradicating vertebrate pest populations (mice, rats and rabbits) on islands. One popular strategy, a sex-reversing drive that converts heterozygous females into sterile males, failed to spread and required the ongoing deployment of gene-drive carriers to achieve eradication. Under alternative strategies, multiplexed gRNAs could overcome inherent polymorphic resistance and were required for eradication success even when the probability of NHEJ was low. Strategies causing homozygotic embryonic non-viability or homozygotic female sterility produced high probabilities of eradication and were robust to NHEJ-mediated deletion of the DNA sequence between multiplexed endonuclease recognition sites. The latter two strategies also purged the gene drive when eradication failed, therefore posing lower long-term risk should animals escape beyond target islands. Multiplexing gRNAs will be necessary if this technology is to be useful for insular extirpation attempts; however, precise knowledge of homing rates will be required to design low-risk gene drives with high probabilities of eradication success.

Footnotes

  • Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3827956.v1.

  • Received April 19, 2017.
  • Accepted July 3, 2017.
  • © 2017 The Author(s)
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16 August 2017
Volume 284, issue 1860
Proceedings of the Royal Society B: Biological Sciences: 284 (1860)
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Keywords

gene drive
homing
non-homologous end joining
resistance allele
population eradication
island conservation
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Dodging silver bullets: good CRISPR gene-drive design is critical for eradicating exotic vertebrates
Thomas A. A. Prowse, Phillip Cassey, Joshua V. Ross, Chandran Pfitzner, Talia A. Wittmann, Paul Thomas
Proc. R. Soc. B 2017 284 20170799; DOI: 10.1098/rspb.2017.0799. Published 9 August 2017
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Research article:

Dodging silver bullets: good CRISPR gene-drive design is critical for eradicating exotic vertebrates

Thomas A. A. Prowse, Phillip Cassey, Joshua V. Ross, Chandran Pfitzner, Talia A. Wittmann, Paul Thomas
Proc. R. Soc. B 2017 284 20170799; DOI: 10.1098/rspb.2017.0799. Published 9 August 2017

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