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The suppressive potential of a gene drive in populations of invasive social wasps is currently limited

Social insects are very successful invasive species, and the continued increase of global trade and transportation has exacerbated this problem. The yellow-legged hornet, Vespa velutina nigrithorax (henceforth Asian hornet), is drastically expanding its range in Western Europe. As an apex insect pre...

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Autores principales: Meiborg, Adriaan B., Faber, Nicky R., Taylor, Benjamin A., Harpur, Brock A., Gorjanc, Gregor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886928/
https://www.ncbi.nlm.nih.gov/pubmed/36717606
http://dx.doi.org/10.1038/s41598-023-28867-8
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author Meiborg, Adriaan B.
Faber, Nicky R.
Taylor, Benjamin A.
Harpur, Brock A.
Gorjanc, Gregor
author_facet Meiborg, Adriaan B.
Faber, Nicky R.
Taylor, Benjamin A.
Harpur, Brock A.
Gorjanc, Gregor
author_sort Meiborg, Adriaan B.
collection PubMed
description Social insects are very successful invasive species, and the continued increase of global trade and transportation has exacerbated this problem. The yellow-legged hornet, Vespa velutina nigrithorax (henceforth Asian hornet), is drastically expanding its range in Western Europe. As an apex insect predator, this hornet poses a serious threat to the honey bee industry and endemic pollinators. Current suppression methods have proven too inefficient and expensive to limit its spread. Gene drives might be an effective tool to control this species, but their use has not yet been thoroughly investigated in social insects. Here, we built a model that matches the hornet’s life history and modelled the effect of different gene drive scenarios on an established invasive population. To test the broader applicability and sensitivity of the model, we also incorporated the invasive European paper wasp Polistes dominula. We find that, due to the haplodiploidy of social hymenopterans, only a gene drive targeting female fertility is promising for population control. Our results show that although a gene drive can suppress a social wasp population, it can only do so under fairly stringent gene drive-specific conditions. This is due to a combination of two factors: first, the large number of surviving offspring that social wasp colonies produce make it possible that, even with very limited formation of resistance alleles, such alleles can quickly spread and rescue the population. Second, due to social wasp life history, infertile individuals do not compete with fertile ones, allowing fertile individuals to maintain a large population size even when drive alleles are widespread. Nevertheless, continued improvements in gene drive technology may make it a promising method for the control of invasive social insects in the future.
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spelling pubmed-98869282023-02-01 The suppressive potential of a gene drive in populations of invasive social wasps is currently limited Meiborg, Adriaan B. Faber, Nicky R. Taylor, Benjamin A. Harpur, Brock A. Gorjanc, Gregor Sci Rep Article Social insects are very successful invasive species, and the continued increase of global trade and transportation has exacerbated this problem. The yellow-legged hornet, Vespa velutina nigrithorax (henceforth Asian hornet), is drastically expanding its range in Western Europe. As an apex insect predator, this hornet poses a serious threat to the honey bee industry and endemic pollinators. Current suppression methods have proven too inefficient and expensive to limit its spread. Gene drives might be an effective tool to control this species, but their use has not yet been thoroughly investigated in social insects. Here, we built a model that matches the hornet’s life history and modelled the effect of different gene drive scenarios on an established invasive population. To test the broader applicability and sensitivity of the model, we also incorporated the invasive European paper wasp Polistes dominula. We find that, due to the haplodiploidy of social hymenopterans, only a gene drive targeting female fertility is promising for population control. Our results show that although a gene drive can suppress a social wasp population, it can only do so under fairly stringent gene drive-specific conditions. This is due to a combination of two factors: first, the large number of surviving offspring that social wasp colonies produce make it possible that, even with very limited formation of resistance alleles, such alleles can quickly spread and rescue the population. Second, due to social wasp life history, infertile individuals do not compete with fertile ones, allowing fertile individuals to maintain a large population size even when drive alleles are widespread. Nevertheless, continued improvements in gene drive technology may make it a promising method for the control of invasive social insects in the future. Nature Publishing Group UK 2023-01-30 /pmc/articles/PMC9886928/ /pubmed/36717606 http://dx.doi.org/10.1038/s41598-023-28867-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Meiborg, Adriaan B.
Faber, Nicky R.
Taylor, Benjamin A.
Harpur, Brock A.
Gorjanc, Gregor
The suppressive potential of a gene drive in populations of invasive social wasps is currently limited
title The suppressive potential of a gene drive in populations of invasive social wasps is currently limited
title_full The suppressive potential of a gene drive in populations of invasive social wasps is currently limited
title_fullStr The suppressive potential of a gene drive in populations of invasive social wasps is currently limited
title_full_unstemmed The suppressive potential of a gene drive in populations of invasive social wasps is currently limited
title_short The suppressive potential of a gene drive in populations of invasive social wasps is currently limited
title_sort suppressive potential of a gene drive in populations of invasive social wasps is currently limited
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886928/
https://www.ncbi.nlm.nih.gov/pubmed/36717606
http://dx.doi.org/10.1038/s41598-023-28867-8
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