A Reduce and Replace Strategy for Suppressing Vector-Borne Diseases: Insights from a Stochastic, Spatial Model

Okamoto, Kenichi W.; Michael, Robert; Lloyd, Alun L.

doi:10.1371/journal.pone.0081860

Cited by 25 publications

(36 citation statements)

References 40 publications

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“…Skeeter Buster has previously been applied to evaluate transgenic control strategies that rely on population reduction ([51] for an FK strategy, and [39] for an RR strategy). These studies found that some wild-type genes can be expected to persist due to inherent stochasticity in the simulation runs.…”

Section: Discussionmentioning

confidence: 99%

Feasible Introgression of an Anti-pathogen Transgene into an Urban Mosquito Population without Using Gene-Drive

2014

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BackgroundIntrogressing anti-pathogen constructs into wild vector populations could reduce disease transmission. It is generally assumed that such introgression would require linking an anti-pathogen gene with a selfish genetic element or similar technologies. Yet none of the proposed transgenic anti-pathogen gene-drive mechanisms are likely to be implemented as public health measures in the near future. Thus, much attention now focuses instead on transgenic strategies aimed at mosquito population suppression, an approach generally perceived to be practical. By contrast, aiming to replace vector competent mosquito populations with vector incompetent populations by releasing mosquitoes carrying a single anti-pathogen gene without a gene-drive mechanism is widely considered impractical.Methodology/Principal FindingsHere we use Skeeter Buster, a previously published stochastic, spatially explicit model of Aedes aegypti to investigate whether a number of approaches for releasing mosquitoes with only an anti-pathogen construct would be efficient and effective in the tropical city of Iquitos, Peru. To assess the performance of such releases using realistic release numbers, we compare the transient and long-term effects of this strategy with two other genetic control strategies that have been developed in Ae. aegypti: release of a strain with female-specific lethality, and a strain with both female-specific lethality and an anti-pathogen gene. We find that releasing mosquitoes carrying only an anti-pathogen construct can substantially decrease vector competence of a natural population, even at release ratios well below that required for the two currently feasible alternatives that rely on population reduction. Finally, although current genetic control strategies based on population reduction are compromised by immigration of wild-type mosquitoes, releasing mosquitoes carrying only an anti-pathogen gene is considerably more robust to such immigration.Conclusions/SignificanceContrary to the widely held view that transgenic control programs aimed at population replacement require linking an anti-pathogen gene to selfish genetic elements, we find releasing mosquitoes in numbers much smaller than those considered necessary for transgenic population reduction can result in comparatively rapid and robust population replacement. In light of this non-intuitive result, directing efforts to improve rearing capacity and logistical support for implementing releases, and reducing the fitness costs of existing recombinant technologies, may provide a viable, alternative route to introgressing anti-pathogen transgenes under field conditions.

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Section: Discussionmentioning

confidence: 99%

Feasible Introgression of an Anti-pathogen Transgene into an Urban Mosquito Population without Using Gene-Drive

2014

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“…Two excellent examples for Aedes aegypti and dengue are [33,34]. Knowing the size of the target population would be crucial in determining the number of released vectors needed to significantly affect gene frequencies.…”

Section: Figurementioning

confidence: 99%

Genetic shifting: a novel approach for controlling vector-borne diseases

Powell

Tabachnick

2014

Trends in Parasitology

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Rendering populations of vectors of diseases incapable of transmitting pathogens through genetic methods has long been a goal of vector geneticists. We outline a method to achieve this goal that does not involve introduction of any new genetic variants to the target population. Rather we propose that shifting the frequencies of naturally occurring alleles that confer refractoriness to transmission can reduce transmission below a sustainable level. The program employs methods successfully used in plant and animal breeding. Because no artificially constructed genetically modified organisms (GMOs) are introduced into the environment, the method is minimally controversial. We use Aedes aegypti and dengue virus (DENV) for illustrative purposes, but point out the proposed program is generally applicable to vector-borne disease control.

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“…Our models predicted that the releases will be more efficient during the dry/cold season when the target population is small (release cohorts represent a larger percentage of the target population; Figure k). The likelihood of fixation of the resistant alleles is also predicted to be higher with smaller target populations (Okamoto et al, ). Analogous to taking advantage of seasonality, traditional vector control methods can actively reduce the wild population size.…”

Section: Discussionmentioning

confidence: 99%

Quantifying the efficacy of genetic shifting in control of mosquito‐borne diseases

Xia

Baskett

Powell

2019

Evolutionary Applications

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Many of the world's most prevalent diseases are transmitted by animal vectors such as dengue transmitted by mosquitoes. To reduce these vector‐borne diseases, a promising approach is “genetic shifting”: selective breeding of the vectors to be more resistant to pathogens and releasing them to the target populations to reduce their ability to transmit pathogens, that is, lower their vector competence. The efficacy of genetic shifting will depend on possible counterforces such as natural selection against low vector competence. To quantitatively evaluate the potential efficacy of genetic shifting, we developed a series of coupled genetic–demographic models that simulate the changes of vector competence during releases of individuals with low vector competence. We modeled vector competence using different genetic architectures, as a multilocus, one‐locus, or two‐locus trait. Using empirically determined estimates of model parameters, the model predicted a reduction of mean vector competence of at least three standard deviations after 20 releases, one release per generation, and 10% of the size of the target population released each time. Sensitivity analysis suggested that release efficacy depends mostly on the vector competence of the released population, release size, release frequency, and the survivorship of the released individuals, with duration of the release program less important. Natural processes such as density‐dependent survival and immigration from external populations also strongly influence release efficacy. Among different sex‐dependent release strategies, releasing blood‐fed females together with males resulted in the highest release efficacy, as these females mate in captivity and reproduce when released, thus contributing a greater proportion of low‐vector‐competence offspring. Conclusions were generally consistent across three models assuming different genetic architectures of vector competence, suggesting that genetic shifting could generally apply to various vector systems and does not require detailed knowledge of the number of loci contributing to vector competence.

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A Reduce and Replace Strategy for Suppressing Vector-Borne Diseases: Insights from a Stochastic, Spatial Model

Cited by 25 publications

References 40 publications

Feasible Introgression of an Anti-pathogen Transgene into an Urban Mosquito Population without Using Gene-Drive

Feasible Introgression of an Anti-pathogen Transgene into an Urban Mosquito Population without Using Gene-Drive

Genetic shifting: a novel approach for controlling vector-borne diseases

Quantifying the efficacy of genetic shifting in control of mosquito‐borne diseases

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