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The potential for a CRISPR gene drive to eradicate or suppress globally invasive social wasps

  • 1.

    Teem, J. L. et al. Genetic biocontrol for invasive species. Front. Bioeng. Biotechnol. 8, 452. https://doi.org/10.3389/fbioe.2020.00452 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  • 2.

    McFarlane, G. R., Whitelaw, C. B. A. & Lillico, S. G. CRISPR-based gene drives for pest control. Trends Biotechnol. 36, 130–133. https://doi.org/10.1016/j.tibtech.2017.10.001 (2018).

    CAS  Article  PubMed  Google Scholar 

  • 3.

    Dearden, P. K. et al. The potential for the use of gene drives for pest control in New Zealand: a perspective. J. R. Soc. N. Z. 48, 225–244. https://doi.org/10.1080/03036758.2017.1385030 (2017).

    Article  Google Scholar 

  • 4.

    Esvelt, K. M., Smidler, A. L., Catteruccia, F. & Church, G. M. Concerning RNA-guided gene drives for the alteration of wild populations. eLife 3, e03401. https://doi.org/10.7554/eLife.03401 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 5.

    Barrangou, R. & Doudna, J. A. Applications of CRISPR technologies in research and beyond. Nat. Biotechnol. 34, 933–941. https://doi.org/10.1038/nbt.3659 (2016).

    CAS  Article  PubMed  Google Scholar 

  • 6.

    Kandul, N. P. et al. Transforming insect population control with precision guided sterile males with demonstration in flies. Nat. Commun. 10, 84. https://doi.org/10.1038/s41467-018-07964-7 (2019).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 7.

    Kyrou, K. et al. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat. Biotechnol. 36, 1062–1066. https://doi.org/10.1038/nbt.4245 (2018).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 8.

    Drury, D. W., Dapper, A. L., Siniard, D. J., Zentner, G. E. & Wade, M. J. CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Sci. Adv. 3, e1601910. https://doi.org/10.1126/sciadv.1601910 (2017).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 9.

    Hammond, A. M. et al. The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLoS Genet. 13, e1007039. https://doi.org/10.1371/journal.pgen.1007039 (2017).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 10.

    Webber, B. L., Raghu, S. & Edwards, O. R. Opinion: is CRISPR-based gene drive a biocontrol silver bullet or global conservation threat?. Proc. Natl. Acad. Sci. U.S.A. 112, 10565–10567. https://doi.org/10.1073/pnas.1514258112 (2015).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 11.

    Wilkins, K. E., Prowse, T. A. A., Cassey, P., Thomas, P. Q. & Ross, J. V. Pest demography critically determines the viability of synthetic gene drives for population control. Math. Biosci. 305, 160–169. https://doi.org/10.1016/j.mbs.2018.09.005 (2018).

    MathSciNet  Article  PubMed  MATH  Google Scholar 

  • 12.

    de la Filia, A. G., Bain, S. A. & Ross, L. Haplodiploidy and the reproductive ecology of Arthropods. Curr. Opin. Insect Sci. 9, 36–43. https://doi.org/10.1016/j.cois.2015.04.018 (2015).

    Article  Google Scholar 

  • 13.

    Deredec, A., Burt, A. & Godfray, H. C. The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179, 2013–2026. https://doi.org/10.1534/genetics.108.089037 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  • 14.

    Rode, N. O., Estoup, A., Bourguet, D., Courtier-Orgogozo, V. & Débarre, F. Population management using gene drive: molecular design, models of spread dynamics and assessment of ecological risks. Conserv. Genet. 20, 671–690. https://doi.org/10.1007/s10592-019-01165-5 (2019).

    CAS  Article  Google Scholar 

  • 15.

    Alphey, N. & Bonsall, M. B. Interplay of population genetics and dynamics in the genetic control of mosquitoes. J. R. Soc. Interface 11, 20131071. https://doi.org/10.1098/rsif.2013.1071 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  • 16.

    Prowse, T. A. A. et al. Dodging silver bullets: good CRISPR gene-drive design is critical for eradicating exotic vertebrates. Proc. R. Soc. B https://doi.org/10.1098/rspb.2017.0799 (2017).

    Article  PubMed  Google Scholar 

  • 17.

    Lowe, S., Browne, M., Boudjelas, S. & De Poorter, M. 100 of the World’s Worst Invasive Alien Species. A Selection from the Global Invasive Species Database Vol. 12 (The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), Auckland, 2000).

    Google Scholar 

  • 18.

    Lester, P. J. & Beggs, J. R. Invasion success and management strategies for social Vespula wasps. Annu. Rev. Entomol. 64, 51–71. https://doi.org/10.1146/annurev-ento-011118-111812 (2019).

    CAS  Article  PubMed  Google Scholar 

  • 19.

    Lester, P. J. et al. Determining the origin of invasions and demonstrating a lack of enemy release from microsporidian pathogens in common wasps (Vespula vulgaris). Divers. Distrib. 20, 964–974. https://doi.org/10.1111/ddi.12223 (2014).

    Article  Google Scholar 

  • 20.

    Harris, R. J. Diet of the wasps Vespula vulgaris and V. germanica in honeydew beech forest of the South Island, New Zealand. N. Z. J. Zool. 18, 159–169 (1991).

    Article  Google Scholar 

  • 21.

    Grangier, J. & Lester, P. J. A novel interference behaviour: invasive wasps remove ants from resources and drop them from a height. Biol. Lett. 7, 664–667. https://doi.org/10.1098/rsbl.2011.0165 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  • 22.

    Wilson, P. R., Karl, B. J., Toft, R. J., Beggs, J. R. & Taylor, R. H. The role of introduced predators and competitors in the decline of kaka (Nestor meridionalis) populations in New Zealand. Biol. Conserv. 83, 175–185. https://doi.org/10.1016/S0006-3207(97)00055-4 (1998).

    Article  Google Scholar 

  • 23.

    Dobelmann, J. et al. Fitness in invasive social wasps: the role of variation in viral load, immune response and paternity in predicting nest size and reproductive output. Oikos 126, 1208–1218. https://doi.org/10.1111/oik.04117 (2017).

    CAS  Article  Google Scholar 

  • 24.

    Sekine, K., Furusawa, T. & Hatakeyama, M. The boule gene is essential for spermatogenesis of haploid insect male. Dev. Biol. 399, 154–163. https://doi.org/10.1016/j.ydbio.2014.12.027 (2015).

    CAS  Article  PubMed  Google Scholar 

  • 25.

    Ferree, P. M. et al. Identification of genes uniquely expressed in the germ-line tissues of the jewel wasp Nasonia vitripennis. G3-Genes Genom. Genet. 5, 2647–2653. https://doi.org/10.1534/g3.115.021386 (2015).

    CAS  Article  Google Scholar 

  • 26.

    Mikhaylova, L. M., Boutanaev, A. M. & Nurminsky, D. I. Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line. Proc. Natl. Acad. Sci. U.S.A. 103, 11975–11980. https://doi.org/10.1073/pnas.0605087103 (2006).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 27.

    Parsch, J., Meiklejohn, C. D., Hauschteck-Jungen, E., Hunziker, P. & Hartl, D. L. Molecular evolution of the ocnus and janus genes in the Drosophila melanogaster species subgroup. Mol. Biol. Evol. 18, 801–811. https://doi.org/10.1093/oxfordjournals.molbev.a003862 (2001).

    CAS  Article  PubMed  Google Scholar 

  • 28.

    Dang, Y. et al. Optimizing sgRNA structure to improve CRISPR-Cas9 knockout efficiency. Genome Biol. 16, 280. https://doi.org/10.1186/s13059-015-0846-3 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 29.

    Yarrington, R. M., Verma, S., Schwartz, S., Trautman, J. K. & Carroll, D. Nucleosomes inhibit target cleavage by CRISPR-Cas9 in vivo. Proc. Natl. Acad. Sci. U.S.A. 115, 9351–9358. https://doi.org/10.1073/pnas.1810062115 (2018).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 30.

    Chaverra-Rodriguez, D. et al. Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing. Nat. Commun. 9, 3008. https://doi.org/10.1038/s41467-018-05425-9 (2018).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 31.

    Noble, C. et al. Daisy-chain gene drives for the alteration of local populations. Proc. Natl. Acad. Sci. U.S.A. 116, 8275–8282. https://doi.org/10.1073/pnas.1716358116 (2019).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 32.

    KaramiNejadRanjbar, M. et al. Consequences of resistance evolution in a Cas9-based sex conversion-suppression gene drive for insect pest management. Proc. Natl. Acad. Sci. U.S.A. 115, 6189–6194. https://doi.org/10.1073/pnas.1713825115 (2018).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 33.

    Brenton-Rule, E. C. et al. The origins of global invasions of the German wasp (Vespula germanica) and its infection with four honey bee viruses. Biol. Invasions 20, 3445–3460. https://doi.org/10.1007/s10530-018-1786-0 (2018).

    Article  Google Scholar 

  • 34.

    Schmack, J. M. et al. Lack of genetic structuring, low effective population sizes and major bottlenecks characterise common and German wasps in New Zealand. Biol. Invasions 21, 3185–3201. https://doi.org/10.1007/s10530-019-02039-0 (2019).

    Article  Google Scholar 

  • 35.

    Tanaka, H., Stone, H. A. & Nelson, D. R. Spatial gene drives and pushed genetic waves. Proc. Natl. Acad. Sci. U.S.A. 114, 8452–8457. https://doi.org/10.1073/pnas.1705868114 (2017).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 36.

    Hammond, A. et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat. Biotechnol. 34, 78–83. https://doi.org/10.1038/nbt.3439 (2016).

    CAS  Article  PubMed  Google Scholar 

  • 37.

    Marshall, J. M., Buchman, A., Sanchez, C. H. & Akbari, O. S. Overcoming evolved resistance to population-suppressing homing-based gene drives. Sci. Rep. 7, 3776. https://doi.org/10.1038/s41598-017-02744-7 (2017).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 38.

    Eckhoff, P. A., Wenger, E. A., Godfray, H. C. & Burt, A. Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics. Proc. Natl. Acad. Sci. U.S.A. 114, E255–E264. https://doi.org/10.1073/pnas.1611064114 (2017).

    CAS  Article  PubMed  Google Scholar 

  • 39.

    North, A., Burt, A. & Godfray, H. C. Modelling the spatial spread of a homing endonuclease gene in a mosquito population. J. Appl. Ecol. 50, 1216–1225. https://doi.org/10.1111/1365-2664.12133 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 40.

    Kirk, N., Kannemeyer, R., Greenaway, A., MacDonald, E. & Stronge, D. Understanding attitudes on new technologies to manage invasive species. Pac. Conserv. Biol. https://doi.org/10.1071/pc18080 (2019).

    Article  Google Scholar 

  • 41.

    Mercier, O. R., KingHunt, A. & Lester, P. J. Novel biotechnologies for eradicating wasps: seeking Māori studies students’ perspectives with Q method. Kōtuitui N. Z. J. Soc. Sci. 14, 136–156. https://doi.org/10.1080/1177083x.2019.1578245 (2019).

    Article  Google Scholar 

  • 42.

    Peters, R. S. et al. Evolutionary history of the Hymenoptera. Curr. Biol. 27, 1013–1018. https://doi.org/10.1016/j.cub.2017.01.027 (2017).

    CAS  Article  PubMed  Google Scholar 

  • 43.

    Stein, K. J. & Fell, R. D. Correlation of queen sperm content with colony size in yellowjackets (Hymenoptera: Vespidae). Environ. Entomol. 23, 1497–1500. https://doi.org/10.1093/ee/23.6.1497 (1994).

    Article  Google Scholar 

  • 44.

    Lester, P. J., Haywood, J., Archer, M. E. & Shortall, C. R. The long-term population dynamics of common wasps in their native and invaded range. J. Anim. Ecol. 86, 337–347. https://doi.org/10.1111/1365-2656.12622 (2017).

    Article  PubMed  Google Scholar 

  • 45.

    Burt, A. & Deredec, A. Self-limiting population genetic control with sex-linked genome editors. Proc. R. Soc. B https://doi.org/10.1098/rspb.2018.0776 (2018).

    Article  PubMed  Google Scholar 

  • 46.

    Prowse, T. A., Adikusuma, F., Cassey, P., Thomas, P. & Ross, J. V. A Y-chromosome shredding gene drive for controlling pest vertebrate populations. eLife 8, e41873. https://doi.org/10.7554/eLife.41873 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  • 47.

    Li, J. et al. Can CRISPR gene drive work in pest and beneficial haplodiploid species?. Evol. Appl. https://doi.org/10.1111/eva.13032 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  • 48.

    Esvelt, K. M. & Gemmell, N. J. Conservation demands safe gene drive. PLoS Biol. 15, e2003850. https://doi.org/10.1371/journal.pbio.2003850 (2017).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 49.

    Piaggio, A. J. et al. Is it time for synthetic biodiversity conservation?. Trends Ecol. Evol. 32, 97–107. https://doi.org/10.1016/j.tree.2016.10.016 (2017).

    Article  PubMed  Google Scholar 

  • 50.

    Edgington, M. P., Harvey-Samuel, T. & Alphey, L. Population-level multiplexing, a promising strategy to manage the evolution of resistance against gene drives targeting a neutral locus. Evol. Appl. https://doi.org/10.1111/eva.12945 (2020).

    Article  Google Scholar 

  • 51.

    Sumner, S., Law, G. & Cini, A. Why we love bees and hate wasps. Ecol. Entomol. 43, 836–845. https://doi.org/10.1111/een.12676 (2018).

    Article  Google Scholar 

  • 52.

    Southon, R. J., Fernandes, O. A., Nascimento, F. S. & Sumner, S. Social wasps are effective biocontrol agents of key lepidopteran crop pests. Proc. R. Soc. B https://doi.org/10.1098/rspb.2019.1676 (2019).

    Article  PubMed  Google Scholar 

  • 53.

    Harris, R. J., Thomas, C. D. & Moller, H. The influence of habitat use and foraging on the replacement of one introduced wasp species by another in New Zealand. Ecol. Entomol. 16, 441–448. https://doi.org/10.1111/j.1365-2311.1991.tb00237.x (1991).

    Article  Google Scholar 

  • 54.

    Lester, P. J. et al. Critical issues facing New Zealand entomology. N. Z. Entomol. 37, 1–13. https://doi.org/10.1080/00779962.2014.861789 (2014).

    Article  Google Scholar 

  • 55.

    Hare, K. M. et al. Intractable: species in New Zealand that continue to decline despite conservation efforts. J. R. Soc. N. Z. 49, 301–319. https://doi.org/10.1080/03036758.2019.1599967 (2019).

    Article  Google Scholar 

  • 56.

    Hu, X. F., Zhang, B., Liao, C. H. & Zeng, Z. J. High-Efficiency CRISPR/Cas9-mediated gene editing in honeybee (Apis mellifera) embryos. G3-Genes Genom. Genet. 9, 1759–1766. https://doi.org/10.1534/g3.119.400130 (2019).

    CAS  Article  Google Scholar 

  • 57.

    Yan, H. et al. An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell 170, 736-747 e739. https://doi.org/10.1016/j.cell.2017.06.051 (2017).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 58.

    Oksanen, J. et al. vegan: community ecology package. (R package version 2.4-0. https://CRAN.R-project.org/package=vegan, 2016).


  • Source: Ecology - nature.com

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