TY - JOUR
T1 - Detecting the population dynamics of an autosomal sex ratio distorter transgene in malariavector mosquitoes
AU - Pollegioni, Paola
AU - North, Ace R.
AU - Persampieri, Tania
AU - Bucci, Alessandro
AU - Minuz, Roxana L.
AU - Groneberg, David Alexander
AU - Nolan, Tony
AU - Papathanos, Philippos Aris
AU - Crisanti, Andrea
AU - Müller, Ruth
N1 - Publisher Copyright:
© 2020 The Authors. Journal of Applied Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society
PY - 2020/10/1
Y1 - 2020/10/1
N2 - The development of genetically modified (GM) mosquitoes and their subsequent field release offers innovative and cost-effective approaches to reduce mosquito-borne diseases, such as malaria. A sex-distorting autosomal transgene has been developed recently in G3 mosquitoes, a laboratory strain of the malaria vector Anopheles gambiae s.l. The transgene expresses an endonuclease called I-PpoI during spermatogenesis, which selectively cleaves the X chromosome to result in ~95% male progeny. Following the World Health Organization guidance framework for the testing of GM mosquitoes, we assessed the dynamics of this transgene in large cages using a joint experimental modelling approach. We performed a 4-month experiment in large, indoor cages to study the population genetics of the transgene. The cages were set up to mimic a simple tropical environment with a diurnal light-cycle, constant temperature and constant humidity. We allowed the generations to overlap to engender a stable age structure in the populations. We constructed a model to mimic the experiments, and used the experimental data to infer the key model parameters. We identified two fitness costs associated with the transgene. First, transgenic adult males have reduced fertility and, second, their female progeny have reduced pupal survival rates. Our results demonstrate that the transgene is likely to disappear in '3 years under our confined conditions. Model predictions suggest this will be true over a wide range of background population sizes and transgene introduction rates. Synthesis and applications. Our study is in line with the World Health Organization guidance recommendations in regard to the development and testing of GM mosquitoes. Since the transgenic sex ratio distorter strain (Ag(PMB)1) has been considered for genetic vector control of malaria, we recorded the dynamics of this transgene in indoor-large cage populations and modelled its post-release persistence under different scenarios. We provide a demonstration of the self-limiting nature of the transgene, and identified new fitness costs that will further reduce the longevity of the transgene after its release. Finally, our study has showcased an alternative and effective statistical method for characterizing the phenotypic expression of a transgene in an insect pest population.
AB - The development of genetically modified (GM) mosquitoes and their subsequent field release offers innovative and cost-effective approaches to reduce mosquito-borne diseases, such as malaria. A sex-distorting autosomal transgene has been developed recently in G3 mosquitoes, a laboratory strain of the malaria vector Anopheles gambiae s.l. The transgene expresses an endonuclease called I-PpoI during spermatogenesis, which selectively cleaves the X chromosome to result in ~95% male progeny. Following the World Health Organization guidance framework for the testing of GM mosquitoes, we assessed the dynamics of this transgene in large cages using a joint experimental modelling approach. We performed a 4-month experiment in large, indoor cages to study the population genetics of the transgene. The cages were set up to mimic a simple tropical environment with a diurnal light-cycle, constant temperature and constant humidity. We allowed the generations to overlap to engender a stable age structure in the populations. We constructed a model to mimic the experiments, and used the experimental data to infer the key model parameters. We identified two fitness costs associated with the transgene. First, transgenic adult males have reduced fertility and, second, their female progeny have reduced pupal survival rates. Our results demonstrate that the transgene is likely to disappear in '3 years under our confined conditions. Model predictions suggest this will be true over a wide range of background population sizes and transgene introduction rates. Synthesis and applications. Our study is in line with the World Health Organization guidance recommendations in regard to the development and testing of GM mosquitoes. Since the transgenic sex ratio distorter strain (Ag(PMB)1) has been considered for genetic vector control of malaria, we recorded the dynamics of this transgene in indoor-large cage populations and modelled its post-release persistence under different scenarios. We provide a demonstration of the self-limiting nature of the transgene, and identified new fitness costs that will further reduce the longevity of the transgene after its release. Finally, our study has showcased an alternative and effective statistical method for characterizing the phenotypic expression of a transgene in an insect pest population.
KW - Ag(PMB)1
KW - anopheles
KW - dynamics
KW - genetically modified
KW - malaria
KW - mosquito
KW - populations
KW - transgene
UR - http://www.scopus.com/inward/record.url?scp=85088146406&partnerID=8YFLogxK
U2 - 10.1111/1365-2664.13702
DO - 10.1111/1365-2664.13702
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AN - SCOPUS:85088146406
SN - 0021-8901
VL - 57
SP - 2086
EP - 2096
JO - Journal of Applied Ecology
JF - Journal of Applied Ecology
IS - 10
ER -