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Mark-release-recapture experiment in Burkina Faso demonstrates reduced fitness and dispersal of genetically-modified sterile malaria mosquitoes.

ABSTRACT: Every year, malaria kills approximately 405,000 people in Sub-Saharan Africa, most of them children under the age of five years. In many countries, progress in malaria control has been threatened by the rapid spread of resistance to antimalarial drugs and insecticides. Novel genetic mosquito control approaches could play an important role in future integrated malaria control strategies. In July 2019, the Target Malaria consortium proceeded with the first release of hemizygous genetically-modified (GM) sterile and non-transgenic sibling males of the malaria mosquito Anopheles coluzzii in Burkina Faso. This study aimed to determine the potential fitness cost associated to the transgene and gather important information related to the dynamic of transgene-carrying mosquitoes, crucial for next development steps. Bayesian estimations confirmed that GM males had lower survival and were less mobile than their wild type (WT) siblings. The estimated male population size in Bana village, at the time of the release was 28,000 - 37,000. These results provide unique information about the fitness and behaviour of released GM males that will inform future releases of more effective strains of the A. gambiae complex.

SUBMITTER: Yao FA

PROVIDER: S-EPMC8831579 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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Mark-release-recapture experiment in Burkina Faso demonstrates reduced fitness and dispersal of genetically-modified sterile malaria mosquitoes.

Yao Franck Adama FA Millogo Abdoul-Azize AA Epopa Patric Stephane PS North Ace A Noulin Florian F Dao Koulmaga K Drabo Mouhamed M Guissou Charles C Kekele Souleymane S Namountougou Moussa M Ouedraogo Robert Kossivi RK Pare Lea L Barry Nourou N Sanou Roger R Wandaogo Haida H Dabire Roch K RK McKemey Andrew A Tripet Frederic F Diabaté Abdoulaye A

Nature communications 20220210 1

Every year, malaria kills approximately 405,000 people in Sub-Saharan Africa, most of them children under the age of five years. In many countries, progress in malaria control has been threatened by the rapid spread of resistance to antimalarial drugs and insecticides. Novel genetic mosquito control approaches could play an important role in future integrated malaria control strategies. In July 2019, the Target Malaria consortium proceeded with the first release of hemizygous genetically-modifie ...[more]

PMID: 35145082

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Project description:Close-kin mark-recapture (CKMR) methods have recently been used to infer demographic parameters such as census population size and survival for fish of interest to fisheries and conservation. These methods have advantages over traditional mark-recapture methods as the mark is genetic, removing the need for physical marking and recapturing that may interfere with parameter estimation. For mosquitoes, the spatial distribution of close-kin pairs has been used to estimate mean dispersal distance, of relevance to vector-borne disease transmission and novel biocontrol strategies. Here, we extend CKMR methods to the life history of mosquitoes and comparable insects. We derive kinship probabilities for mother-offspring, father-offspring, full-sibling and half-sibling pairs, where an individual in each pair may be a larva, pupa or adult. A pseudo-likelihood approach is used to combine the marginal probabilities of all kinship pairs. To test the effectiveness of this approach at estimating mosquito demographic parameters, we develop an individual-based model of mosquito life history incorporating egg, larva, pupa and adult life stages. The simulation labels each individual with a unique identification number, enabling close-kin relationships to be inferred for sampled individuals. Using the dengue vector Aedes aegypti as a case study, we find the CKMR approach provides unbiased estimates of adult census population size, adult and larval mortality rates, and larval life stage duration for logistically feasible sampling schemes. Considering a simulated population of 3,000 adult mosquitoes, estimation of adult parameters is accurate when ca. 40 adult females are sampled biweekly over a three month period. Estimation of larval parameters is accurate when adult sampling is supplemented with ca. 120 larvae sampled biweekly over the same period. The methods are also effective at detecting intervention-induced increases in adult mortality and decreases in population size. As the cost of genome sequencing declines, CKMR holds great promise for characterizing the demography of mosquitoes and comparable insects of epidemiological and agricultural significance.

Project description:BACKGROUND:Understanding the dispersal dynamics of invasive mosquito species is fundamental to improve vector surveillance and to target control efforts. Aedes albopictus has been deemed a poor flyer as its range of active dispersal is generally assumed to be limited to a few hundred metres, while laboratory studies suggest this mosquito could actually fly several kilometres. The discrepancy may be due to differences in the local environment or to the methodological approach. In Switzerland, Ae. albopictus has been present since 2003 and has since then expanded its range. While passive dispersal is a key driver, it remains unclear how far this mosquito spreads through active flight and what the age structure and size of the local population are, all important parameters for vector surveillance and control. METHOD:We investigated the active dispersal, daily survival rate and population size of Ae. albopictus in mark-release-recapture studies in Coldrerio and Lugano, two areas of intensive control in Switzerland. To mark mosquitoes emerging from breeding sites, we used self-marking units with fluorescent pigment that have minimal impact on mosquito survival and behaviour. We recaptured the adult mosquitoes with BG-Sentinel traps within a radius of 1 km from the marking units over 22 consecutive days. RESULTS:We found that 77.5% of the recaptured Ae. albopictus individuals flew further than 250 m, the limit that is usually deemed sufficient for vector containment. The average age of females and males was 8.6 days and 7.8 days in Coldrerio and Lugano, respectively, while the estimated mosquito population densities were 134 mosquitoes/ha in Coldrerio and 767 mosquitoes/ha in Lugano. CONCLUSIONS:Self-marking units are an effective tool to mark wild mosquitoes. Using this approach, we found that mosquitoes survive long enough to potentially transmit arboviral disease in our study area and that host-seeking Ae. albopictus females may travel further than previously assumed for European mosquito populations. This finding has direct implications for vector control as emergency treatments around positive cases, as well as surveillance and control around detections of new infestations, might need to be extended beyond the usual recommended range of just a few hundred metres.

Project description:BackgroundThe sterile insect technique (SIT), which involves area-wide inundative releases of sterile insects to suppress the reproduction of a target species, has proven to be an effective pest control method. The technique demands the continuous release of sterilized insects in quantities that ensure a high sterile male:wild male ratio for the suppression of the wild population over succeeding generations.MethodsFor these releases, it is important to determine several ecological and biological population parameters, including the longevity of the released males in the field, the dispersal of the released males and the wild pest population size. The Lee County Mosquito Control District initiated a study in a 47-ha portion of Captiva Island (Florida, USA), an island with a total area of 230 ha, to define biological SIT parameters for Aedes aegypti (L.), an invasive disease-vectoring mosquito known to be difficult to control due to a combination of daytime biting activity, use of cryptic breeding habitats that are difficult to target with conventional night-time ultra-low volume methods, and emerging resistance to commonly used insecticides. Another goal was to assess patterns of dispersal and survival for laboratory-reared sterile Ae. aegypti males released over time in the pilot site. These parameters will be used to evaluate the efficacy of a SIT suppression program for Ae. aegypti on Captiva Island.ResultsOver the course of seven mark-release-recapture studies using single- and multiple-point releases, 190,504 sterile marked males were released, for which the recapture rate was 1.5% over a mean period of 12 days. The mean distance traveled by sterile males of the local strain of Ae. aegypti that has colonized Captiva Island was 201.7 m from the release point, with an observed maximum traveled distance of 404.5 m. The released sterile mosquitoes had a probability of daily survival of 0.67 and an average life expectancy of ~ 2.46 days.ConclusionsThese data together with the population size estimate and sterile:wild ratio provide a solid basis for planning the SIT operational phase which is aimed at mosquito population suppression.

Project description:Close-kin mark-recapture (CKMR) is a method for estimating abundance and vital rates from kinship relationships observed in genetic samples. CKMR inference only requires animals to be sampled once (e.g., lethally), potentially widening the scope of population-level inference relative to traditional monitoring programs.One assumption of CKMR is that, conditional on individual covariates like age, all animals have an equal probability of being sampled. However, if genetic data are collected opportunistically (e.g., via hunters or fishers), there is potential for spatial variation in sampling probability that can bias CKMR estimators, particularly when genetically related individuals stay in close proximity.We used individual-based simulation to investigate consequences of dispersal limitation and spatially biased sampling on performance of naive (nonspatial) CKMR estimators of abundance, fecundity, and adult survival. Population dynamics approximated that of a long-lived mammal species subject to lethal sampling.Naive CKMR abundance estimators were relatively unbiased when dispersal was unconstrained (i.e., complete mixing) or when sampling was random or subject to moderate levels of spatial variation. When dispersal was limited, extreme variation in spatial sampling probabilities negatively biased abundance estimates. Reproductive schedules and survival were well estimated, except for survival when adults could emigrate out of the sampled area. Incomplete mixing was readily detected using Kolmogorov-Smirnov tests.Although CKMR appears promising for estimating abundance and vital rates with opportunistically collected genetic data, care is needed when dispersal limitation is coupled with spatially biased sampling. Fortunately, incomplete mixing is easily detected with adequate sample sizes. In principle, it is possible to devise and fit spatially explicit CKMR models to avoid bias under dispersal limitation, but development of such models necessitates additional complexity (and possibly additional data). We suggest using simulation studies to examine potential bias and precision of proposed modeling approaches prior to implementing a CKMR program.

Project description:Vector control is a major component of the malaria control strategy. The increasing spread of insecticide resistance has encouraged the development of new tools such as genetic control which use releases of modified male mosquitoes. The use of male mosquitoes as part of a control strategy requires an improved understanding of male mosquito biology, including the factors influencing their survival and dispersal, as well as the ability to accurately estimate the size of a target mosquito population. This study was designed to determine the seasonal variation in population size via repeated mark-release-recapture experiments and to estimate the survival and dispersal of male mosquitoes of the Anopheles gambiae complex in a small west African village.Mark-release-recapture experiments were carried out in Bana Village over two consecutive years, during the wet and the dry seasons. For each experiment, around 5000 (3407-5273) adult male Anopheles coluzzii mosquitoes were marked using three different colour dye powders (red, blue and green) and released in three different locations in the village (centre, edge and outside). Mosquitoes were recaptured at sites spread over the village for seven consecutive days following the releases. Three different capture methods were used: clay pots, pyrethroid spray catches and swarm sampling.Swarm sampling was the most productive method for recapturing male mosquitoes in the field. Population size and survival were estimated by Bayesian analyses of the Fisher-Ford model, revealing an about 10-fold increase in population size estimates between the end of dry season (10,000-50,000) to the wet season (100,000-500,000). There were no detectable seasonal effects on mosquito survival, suggesting that factors other than weather may play an important role. Mosquito dispersal ranged from 40 to 549 m over the seven days of each study and was not influenced by the season, but mainly by the release location, which explained more than 44% of the variance in net dispersal distance.This study clearly shows that male-based MRR experiments can be used to estimate some parameters of wild male populations such as population size, survival, and dispersal and to estimate the spatial patterns of movement in a given locality.

Project description:BackgroundReproductive containment provides an opportunity to implement a staged-release strategy for genetic control of malaria vectors, in particular allowing predictions about the spread and persistence of (self-limiting) sterile and male-biased strains to be compared to outcomes before moving to (self-sustaining) gene-drive strains.MethodsIn this study, we: (i) describe a diffusion-advection-reaction model of the spread and persistence of a single cohort of male mosquitoes; (ii) elicit informative prior distributions for model parameters, for wild-type (WT) and genetically modified dominant sterile strains (DSM); (iii) estimate posterior distributions for WT strains using data from published mark-recapture-release (MRR) experiments, with inference performed through the Delayed-Rejection Adaptive Metropolis algorithm; and (iv) weight prior distributions, in order to make predictions about genetically modified strains using Bayes factors calculated for the WT strains.ResultsIf a single cohort of 5000 genetically modified dominant sterile male mosquitoes are released at the same location as previous MRR experiments with their WT counterparts, there is a 90% probability that the expected number of released mosquitoes will fall to < 1 in 10 days, and that by 12 days there will be a 99% probability that no mosquitoes will be found more than 150 m from the release location.ConclusionsSpread and persistence models should form a key component of risk assessments of novel genetic control strategies for malaria vectors. Our predictions, used in an independent risk assessment, suggest that genetically modified sterile male mosquitoes will remain within the locality of the release site, and that they will persist for a very limited amount of time. Data gathered following the release of these mosquitoes will enable us to test the accuracy of these predictions and also provide a means to update parameter distributions for genetic strains in a coherent (Bayesian) framework. We anticipate this will provide additional insights about how to conduct probabilistic risk assessments of stage-released genetically modified mosquitoes.

Dataset Information

Mark-release-recapture experiment in Burkina Faso demonstrates reduced fitness and dispersal of genetically-modified sterile malaria mosquitoes.

Publications

Mark-release-recapture experiment in Burkina Faso demonstrates reduced fitness and dispersal of genetically-modified sterile malaria mosquitoes.

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