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Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control
BACKGROUND: Release of gene-drive mutants to suppress Anopheles mosquito reproduction is a promising method of malaria control. However, many scientific, regulatory and ethical questions remain before transgenic mosquitoes can be utilised in the field. At a behavioural level, gene-drive carrying mut...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7539510/ https://www.ncbi.nlm.nih.gov/pubmed/33028410 http://dx.doi.org/10.1186/s13071-020-04382-x |
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author | Su, Matthew P. Georgiades, Marcos Bagi, Judit Kyrou, Kyros Crisanti, Andrea Albert, Joerg T. |
author_facet | Su, Matthew P. Georgiades, Marcos Bagi, Judit Kyrou, Kyros Crisanti, Andrea Albert, Joerg T. |
author_sort | Su, Matthew P. |
collection | PubMed |
description | BACKGROUND: Release of gene-drive mutants to suppress Anopheles mosquito reproduction is a promising method of malaria control. However, many scientific, regulatory and ethical questions remain before transgenic mosquitoes can be utilised in the field. At a behavioural level, gene-drive carrying mutants should be at least as sexually attractive as the wildtype populations they compete against, with a key element of Anopheles copulation being acoustic courtship. We analysed sound emissions and acoustic preference in a doublesex mutant previously used to collapse Anopheles gambiae (s.l.) cages. METHODS: Anopheles rely on flight tones produced by the beating of their wings for acoustic mating communication. We assessed the impact of disrupting a female-specific isoform of the doublesex gene (dsxF) on the wing beat frequency (WBF; measured as flight tone) of males (XY) and females (XX) in homozygous dsxF(−) mutants (dsxF(−/−)), heterozygous dsxF(−) carriers (dsxF(+/−)) and G3 dsxF(+) controls (dsxF(+/+)). To exclude non-genetic influences, we controlled for temperature and wing length. We used a phonotaxis assay to test the acoustic preferences of mutant and control mosquitoes. RESULTS: A previous study showed an altered phenotype only for dsxF(−/−) females, who appear intersex, suggesting that the female-specific dsxF allele is haplosufficient. We identified significant, dose-dependent increases in the WBF of both dsxF(−/−) and dsxF(+/−) females compared to dsxF(+/+) females. All female WBFs remained significantly lower than male equivalents, though. Males showed stronger phonotactic responses to the WBFs of control dsxF(+/+) females than to those of dsxF(+/−) and dsxF(−/−) females. We found no evidence of phonotaxis in any female genotype. No male genotypes displayed any deviations from controls. CONCLUSIONS: A prerequisite for anopheline copulation is the phonotactic attraction of males towards female flight tones within mating swarms. Reductions in mutant acoustic attractiveness diminish their mating efficiency and thus the efficacy of population control efforts. Caged population assessments may not successfully reproduce natural mating scenarios. We propose to amend existing testing protocols to better reflect competition between mutants and target populations. Our findings confirm that dsxF disruption has no effect on males; for some phenotypic traits, such as female WBFs, the effects of dsxF appear dose-dependent rather than haplosufficient. [Image: see text] |
format | Online Article Text |
id | pubmed-7539510 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-75395102020-10-08 Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control Su, Matthew P. Georgiades, Marcos Bagi, Judit Kyrou, Kyros Crisanti, Andrea Albert, Joerg T. Parasit Vectors Research BACKGROUND: Release of gene-drive mutants to suppress Anopheles mosquito reproduction is a promising method of malaria control. However, many scientific, regulatory and ethical questions remain before transgenic mosquitoes can be utilised in the field. At a behavioural level, gene-drive carrying mutants should be at least as sexually attractive as the wildtype populations they compete against, with a key element of Anopheles copulation being acoustic courtship. We analysed sound emissions and acoustic preference in a doublesex mutant previously used to collapse Anopheles gambiae (s.l.) cages. METHODS: Anopheles rely on flight tones produced by the beating of their wings for acoustic mating communication. We assessed the impact of disrupting a female-specific isoform of the doublesex gene (dsxF) on the wing beat frequency (WBF; measured as flight tone) of males (XY) and females (XX) in homozygous dsxF(−) mutants (dsxF(−/−)), heterozygous dsxF(−) carriers (dsxF(+/−)) and G3 dsxF(+) controls (dsxF(+/+)). To exclude non-genetic influences, we controlled for temperature and wing length. We used a phonotaxis assay to test the acoustic preferences of mutant and control mosquitoes. RESULTS: A previous study showed an altered phenotype only for dsxF(−/−) females, who appear intersex, suggesting that the female-specific dsxF allele is haplosufficient. We identified significant, dose-dependent increases in the WBF of both dsxF(−/−) and dsxF(+/−) females compared to dsxF(+/+) females. All female WBFs remained significantly lower than male equivalents, though. Males showed stronger phonotactic responses to the WBFs of control dsxF(+/+) females than to those of dsxF(+/−) and dsxF(−/−) females. We found no evidence of phonotaxis in any female genotype. No male genotypes displayed any deviations from controls. CONCLUSIONS: A prerequisite for anopheline copulation is the phonotactic attraction of males towards female flight tones within mating swarms. Reductions in mutant acoustic attractiveness diminish their mating efficiency and thus the efficacy of population control efforts. Caged population assessments may not successfully reproduce natural mating scenarios. We propose to amend existing testing protocols to better reflect competition between mutants and target populations. Our findings confirm that dsxF disruption has no effect on males; for some phenotypic traits, such as female WBFs, the effects of dsxF appear dose-dependent rather than haplosufficient. [Image: see text] BioMed Central 2020-10-07 /pmc/articles/PMC7539510/ /pubmed/33028410 http://dx.doi.org/10.1186/s13071-020-04382-x Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Su, Matthew P. Georgiades, Marcos Bagi, Judit Kyrou, Kyros Crisanti, Andrea Albert, Joerg T. Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control |
title | Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control |
title_full | Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control |
title_fullStr | Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control |
title_full_unstemmed | Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control |
title_short | Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control |
title_sort | assessing the acoustic behaviour of anopheles gambiae (s.l.) dsxf mutants: implications for vector control |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7539510/ https://www.ncbi.nlm.nih.gov/pubmed/33028410 http://dx.doi.org/10.1186/s13071-020-04382-x |
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