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Mating harassment may boost the effectiveness of the sterile insect technique for Aedes mosquitoes.

ABSTRACT: The sterile insect technique is based on the overflooding of a target population with released sterile males inducing sterility in the wild female population. It has proven to be effective against several insect pest species of agricultural and veterinary importance and is under development for Aedes mosquitoes. Here, we show that the release of sterile males at high sterile male to wild female ratios may also impact the target female population through mating harassment. Under laboratory conditions, male to female ratios above 50 to 1 reduce the longevity of female Aedes mosquitoes by reducing their feeding success. Under controlled conditions, blood uptake of females from an artificial host or from a mouse and biting rates on humans are also reduced. Finally, in a field trial conducted in a 1.17 ha area in China, the female biting rate is reduced by 80%, concurrent to a reduction of female mosquito density of 40% due to the swarming of males around humans attempting to mate with the female mosquitoes. This suggests that the sterile insect technique does not only suppress mosquito vector populations through the induction of sterility, but may also reduce disease transmission due to increased female mortality and lower host contact.

SUBMITTER: Zhang D

PROVIDER: S-EPMC10912119 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

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Mating harassment may boost the effectiveness of the sterile insect technique for Aedes mosquitoes.

Zhang Dongjing D Maiga Hamidou H Li Yongjun Y Bakhoum Mame Thierno MT Wang Gang G Sun Yan Y Damiens David D Mamai Wadaka W Bimbilé Somda Nanwintoum Séverin NS Wallner Thomas T Bueno-Masso Odet O Martina Claudia C Kotla Simran Singh SS Yamada Hanano H Lu Deng D Tan Cheong Huat CH Guo Jiatian J Feng Qingdeng Q Zhang Junyan J Zhao Xufei X Paerhande Dilinuer D Pan Wenjie W Wu Yu Y Zheng Xiaoying X Wu Zhongdao Z Xi Zhiyong Z Vreysen Marc J B MJB Bouyer Jérémy J

Nature communications 20240304 1

The sterile insect technique is based on the overflooding of a target population with released sterile males inducing sterility in the wild female population. It has proven to be effective against several insect pest species of agricultural and veterinary importance and is under development for Aedes mosquitoes. Here, we show that the release of sterile males at high sterile male to wild female ratios may also impact the target female population through mating harassment. Under laboratory condit ...[more]

PMID: 38438367

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Project description:Novel and alternative vector control approaches using a sterile male-based release to suppress Aedes aegypti mosquito vectors have recently been tested in the field in many countries. These approaches included the sterile insect technique (SIT), incompatible insect technique (IIT), and a combination of both techniques. In this study, we conducted a series of experiments to compare the quality between radiation-based and Wolbachia-induced sterile males in terms of flight ability, sterility, mating competitiveness, survival rate, and longevity. Aedes aegypti mosquitoes irradiated at 50 Gy (SIT) and those trans-infected with wAlbB Wolbachia (IIT) were used for quality comparison. Our results showed that irradiated and Wolbachia trans-infected males were not significantly different in flight ability (p > 0.05) and both could induce sterility in wild-type females. In addition, although irradiation at 50 Gy or Wolbachia trans-infection reduced male mating competitiveness, combined irradiation and Wolbachia wAlbB trans-infection increased male competitiveness at the one-to-one ratio. Increasing the number of sterile males released could compensate for reduced competitiveness but it does not make them more competitive. Irradiation did not affect the survival and longevity of irradiated males, but it showed significant negative impacts on females (p < 0.05); while the opposite was observed in the case of Wolbachia infection, i.e., with significant increase in the survival rate of Wolbachia trans-infected males (p < 0.05), but both survival and longevity were reduced in Wolbachia trans-infected females with no significant impacts (p > 0.05). In conclusion, neither irradiation nor Wolbachia trans-infection significantly affected the quality of sterile males except their mating competitiveness; but this could compensate by increasing the number of sterile males released. Sterility could be induced by either 50 Gy irradiation or wAlbB trans-infection. Mating competitiveness results showed that a higher number of sterile males produced by irradiation need to be released in comparison to those produced by Wolbachia trans-infection. Our results should be useful for planning SIT, IIT, or a combination for Ae. aegypti vector control.

Project description:Combination of the sterile insect technique with the incompatible insect technique is considered to be a safe approach to control Aedes albopictus populations in the absence of an accurate and scalable sex separation system or genetic sexing strain. Our previous study has shown that the triple Wolbachia-infected Ae. albopictus strain (wAlbA, wAlbB and wPip) was suitable for mass rearing and females could be completely sterilized as pupae with a radiation dose of at least 28 Gy. However, whether this radiation dose can influence the mating competitiveness of the triple infected males was still unknown. In this study we aimed to evaluate the effects of irradiation on the male mating competitiveness of the triple infected strain under laboratory and semi-field conditions. The results herein indicate that irradiation with a lower, female-sterilizing dose has no negative impact on the longevity of triple infected males while a reduced lifespan was observed in the wild type males (wAlbA and wAlbB) irradiated with a higher male-sterilizing dose, in small cages. At different sterile: fertile release ratios in small cages, triple-infected males induced 39.8, 81.6 and 87.8% sterility in a wild type female population at 1:1, 5:1 and 10:1 release ratios, respectively, relative to a fertile control population. Similarly, irradiated triple infected males induced 31.3, 70.5 and 89.3% sterility at 1:1, 5:1 and 10:1 release ratios, respectively, again relative to the fertile control. Under semi-field conditions at a 5:1 release ratio, relative to wild type males, the mean male mating competitiveness index of 28 Gy irradiated triple-infected males was significantly higher than 35 Gy irradiated wild type males, while triple infected males showed no difference in mean mating competitiveness to either irradiated triple-infected or irradiated wild type males. An unexpected difference was also observed in the relative male mating competitiveness of the triple infected strain after irradiation at 28 Gy dose in small vs large cages, with a higher male mating competitiveness index calculated from results of experiments in the large cages. Based on these results, we consider that the male mating performance of the triple infected strain after irradiation at 28 Gy, a dose required for complete female sterility and the avoidance of population replacement, is approximately equal to that of the wild type males under semi-field conditions. Though field evaluation is required, this suggests that the triple infected strain is suitable for irradiation and release as part of a combined SIT-IIT approach to Ae. albopictus control.

Project description:BackgroundThe invasive species Aedes albopictus, commonly known as the Asian tiger mosquito, has undergone extreme range expansion by means of steady introductions as blind passengers in vehicles traveling from the Mediterranean to south-west Germany. The more than 25 established populations in the State of Baden-Württemberg, Palatine and Hesse (south-west Germany) have become a major nuisance and public health threat. Aedes albopictus deserves special attention as a vector of arboviruses, including dengue, chikungunya and Zika viruses. In Germany, Ae. albopictus control programs are implemented by local communities under the auspices of health departments and regulatory offices.MethodsThe control strategy comprised three pillars: (i) community participation (CP) based on the elimination of breeding sites or improved environmental sanitation, using fizzy tablets based on Bacillus thuringiensis israelensis (fizzy Bti tablets; Culinex® Tab plus); (ii) door-to-door (DtD) control by trained staff through the application of high doses of a water-dispersible Bti granular formulation (Vectobac® WG) aimed at achieving a long-lasting killing effect; and (iii) implementation of the sterile insect technique (SIT) to eliminate remaining Ae. albopictus populations. Prior to initiating large-scale city-wide treatments on a routine basis, the efficacy of the three elements was evaluated in laboratory and semi-field trials. Special emphasis was given to the mass release of sterile Ae. albopictus males.ResultsMore than 60% of the local residents actively participated in the first pillar (CP) of the large-scale control program. The most effective element of the program was found to be the DtD intervention, including the application of Vectobac® WG (3000 ITU/mg) to potential breeding sites (10 g per rainwater container, maximum of 200 l = maximum of approx. 150,000 ITU/l, and 2.5 g per container < 50 l) with a persistence of at least 3 weeks. In Ludwigshafen, larval source management resulted in a Container Index for Ae. albopictus of < 1% in 2020 compared to 10.9% in 2019. The mean number of Aedes eggs per ovitrap per 2 weeks was 4.4 in Ludwigshafen, 18.2 in Metzgergrün (Freiburg) (SIT area) and 22.4 in the control area in Gartenstadt (Freiburg). The strong reduction of the Ae. albopictus population by Bti application was followed by weekly releases of 1013 (Ludwigshafen) and 2320 (Freiburg) sterile Ae. albopictus males per hectare from May until October, resulting in a high percentage of sterile eggs. In the trial areas of Ludwigshafen and Frieburg, egg sterility reached 84.7 ± 12.5% and 62.7 ± 25.8%, respectively; in comparison, the natural sterility in the control area was 14.6 ± 7.3%. The field results were in line with data obtained in cage tests under laboratory conditions where sterility rates were 87.5 ± 9.2% after wild females mated with sterile males; in comparison, the sterility of eggs laid by females mated with unirradiated males was only 3.3 ± 2.8%. The overall egg sterility of about 84% in Ludwigshafen indicates that our goal to almost eradicate the Ae. albopictus population could be achieved. The time for inspection and treatment of a single property ranged from 19 to 26 min depending on the experience of the team and costs 6-8 euros per property.ConclusionsIt is shown that an integrated control program based on a strict monitoring scheme can be most effective when it comprises three components, namely CP, DtD intervention that includes long-lasting Bti-larviciding to strongly reduce Ae. albopictus populations and SIT to reduce the remaining Ae. albopictus population to a minimum or even to eradicate it. The combined use of Bti and SIT is the most effective and selective tool against Ae. albopictus, one of the most dangerous mosquito vector species.

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Mating harassment may boost the effectiveness of the sterile insect technique for Aedes mosquitoes.

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Mating harassment may boost the effectiveness of the sterile insect technique for Aedes mosquitoes.

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