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Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains

BACKGROUND: Evaluating and improving mating success and competitive ability of laboratory-reared transgenic mosquito strains will enhance the effectiveness of proposed disease-control strategies that involve deployment of transgenic strains. Two components of the mosquito rearing process, larval die...

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Autores principales: Aldersley, Andrew, Pongsiri, Arissara, Bunmee, Kamonchanok, Kijchalao, Udom, Chittham, Wachiraphan, Fansiri, Thanyalak, Pathawong, Nattaphol, Qureshi, Alima, Harrington, Laura C., Ponlawat, Alongkot, Cator, Lauren J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6642483/
https://www.ncbi.nlm.nih.gov/pubmed/31324262
http://dx.doi.org/10.1186/s13071-019-3617-2
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author Aldersley, Andrew
Pongsiri, Arissara
Bunmee, Kamonchanok
Kijchalao, Udom
Chittham, Wachiraphan
Fansiri, Thanyalak
Pathawong, Nattaphol
Qureshi, Alima
Harrington, Laura C.
Ponlawat, Alongkot
Cator, Lauren J.
author_facet Aldersley, Andrew
Pongsiri, Arissara
Bunmee, Kamonchanok
Kijchalao, Udom
Chittham, Wachiraphan
Fansiri, Thanyalak
Pathawong, Nattaphol
Qureshi, Alima
Harrington, Laura C.
Ponlawat, Alongkot
Cator, Lauren J.
author_sort Aldersley, Andrew
collection PubMed
description BACKGROUND: Evaluating and improving mating success and competitive ability of laboratory-reared transgenic mosquito strains will enhance the effectiveness of proposed disease-control strategies that involve deployment of transgenic strains. Two components of the mosquito rearing process, larval diet quantity and aquatic environment - which are linked to physiological and behavioural differences in adults - are both relatively easy to manipulate. In mosquitoes, as for many other arthropod species, the quality of the juvenile habitat is strongly associated with adult fitness characteristics, such as longevity and fecundity. However, the influence of larval conditioning on mating performance is poorly understood. Here, we investigated the combined effects of larval diet amount and environmental water source on adult male mating success in a genetically modified strain of Aedes aegypti mosquitoes in competition with wild-type conspecifics. Importantly, this research was conducted in a field setting using low generation laboratory and wild-type lines. RESULTS: By controlling larval diet (high and low) and rearing water source (field-collected and laboratory water), we generated four treatment lines of a genetically modified strain of Ae. aegypti tagged with fluorescent sperm. Laboratory reared mosquitoes were then competed against a low generation wild-type colony in a series of laboratory and semi-field mating experiments. While neither food quantity nor larval aquatic environment were found to affect male mating fitness, the transgenic lines consistently outperformed wild-types in laboratory competition assays, an advantage that was not conferred to semi-field tests. CONCLUSIONS: Using a model transgenic system, our results indicate that differences in the experimental conditions of laboratory- and field-based measures of mating success can lead to variation in the perceived performance ability of modified strains if they are only tested in certain environments. While there are many potential sources of variation between laboratory and field lines, laboratory adaptation - which may occur over relatively few generations in this species - may directly impact mating ability depending on the context in which it is measured. We suggest that colony-hybridization with field material can potentially be used to mitigate these effects in a field setting. Release programs utilising mass-produced modified laboratory strains should incorporate comparative assessments of quality in candidate lines. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3617-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-66424832019-07-29 Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains Aldersley, Andrew Pongsiri, Arissara Bunmee, Kamonchanok Kijchalao, Udom Chittham, Wachiraphan Fansiri, Thanyalak Pathawong, Nattaphol Qureshi, Alima Harrington, Laura C. Ponlawat, Alongkot Cator, Lauren J. Parasit Vectors Research BACKGROUND: Evaluating and improving mating success and competitive ability of laboratory-reared transgenic mosquito strains will enhance the effectiveness of proposed disease-control strategies that involve deployment of transgenic strains. Two components of the mosquito rearing process, larval diet quantity and aquatic environment - which are linked to physiological and behavioural differences in adults - are both relatively easy to manipulate. In mosquitoes, as for many other arthropod species, the quality of the juvenile habitat is strongly associated with adult fitness characteristics, such as longevity and fecundity. However, the influence of larval conditioning on mating performance is poorly understood. Here, we investigated the combined effects of larval diet amount and environmental water source on adult male mating success in a genetically modified strain of Aedes aegypti mosquitoes in competition with wild-type conspecifics. Importantly, this research was conducted in a field setting using low generation laboratory and wild-type lines. RESULTS: By controlling larval diet (high and low) and rearing water source (field-collected and laboratory water), we generated four treatment lines of a genetically modified strain of Ae. aegypti tagged with fluorescent sperm. Laboratory reared mosquitoes were then competed against a low generation wild-type colony in a series of laboratory and semi-field mating experiments. While neither food quantity nor larval aquatic environment were found to affect male mating fitness, the transgenic lines consistently outperformed wild-types in laboratory competition assays, an advantage that was not conferred to semi-field tests. CONCLUSIONS: Using a model transgenic system, our results indicate that differences in the experimental conditions of laboratory- and field-based measures of mating success can lead to variation in the perceived performance ability of modified strains if they are only tested in certain environments. While there are many potential sources of variation between laboratory and field lines, laboratory adaptation - which may occur over relatively few generations in this species - may directly impact mating ability depending on the context in which it is measured. We suggest that colony-hybridization with field material can potentially be used to mitigate these effects in a field setting. Release programs utilising mass-produced modified laboratory strains should incorporate comparative assessments of quality in candidate lines. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3617-2) contains supplementary material, which is available to authorized users. BioMed Central 2019-07-19 /pmc/articles/PMC6642483/ /pubmed/31324262 http://dx.doi.org/10.1186/s13071-019-3617-2 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research
Aldersley, Andrew
Pongsiri, Arissara
Bunmee, Kamonchanok
Kijchalao, Udom
Chittham, Wachiraphan
Fansiri, Thanyalak
Pathawong, Nattaphol
Qureshi, Alima
Harrington, Laura C.
Ponlawat, Alongkot
Cator, Lauren J.
Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains
title Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains
title_full Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains
title_fullStr Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains
title_full_unstemmed Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains
title_short Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains
title_sort too “sexy” for the field? paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of aedes aegypti transgenic strains
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6642483/
https://www.ncbi.nlm.nih.gov/pubmed/31324262
http://dx.doi.org/10.1186/s13071-019-3617-2
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