Temasek Life Sciences Laboratory, National University of Singapore, Singapore, 117604, Singapore.
Present address: Institute of Infectious Disease, Shenzhen Bay Laboratory, Shenzhen, 518000, China.
BMC Biol. 2023 Nov 27;21(1):274. doi: 10.1186/s12915-023-01757-1.
Aedes aegypti (Ae. aegypti) is the major vector that transmits many diseases including dengue, Zika, and filariasis in tropical and subtropical regions. Due to the growing resistance to chemical-based insecticides, biological control methods have become an emerging direction to control mosquito populations. The sterile insect technique (SIT) deploys high doses of ionizing radiation to sterilize male mosquitoes before the release. The Wolbachia-based population suppression method of the incompatible insect technique (IIT) involves the release of Wolbachia-infected males to sterilize uninfected field females. Due to the lack of perfect sex separation tools, a low percentage of female contamination is detected in the male population. To prevent the unintentional release of these Wolbachia-infected females which might result in population replacement, a low dose of X-ray irradiation is deployed to sterilize any female escapees. However, it remains unclear whether these irradiation-induced male and female sterilizations share common mechanisms.
In this work, we set out to define the minimum dose of X-ray radiation required for complete female sterilization in Ae. aegypti (NEA-EHI strain). Further results showed that this minimum dose of X-ray irradiation for female sterilization significantly reduced male fertility. Similar results have been reported previously in several operational trials. By addressing the underlying causes of the sterility, our results showed that male sterility is likely due to chromosomal damage in the germ cells induced by irradiation. In contrast, female sterility appears to differ and is likely initiated by the elimination of the somatic supporting cells, which results in the blockage of the ovariole maturation. Building upon these findings, we identified the minimum dose of X-ray irradiation on the Wolbachia-infected NEA-EHI (wAlbB-SG) strain, which is currently being used in the IIT-SIT field trial. Compared to the uninfected parental strain, a lower irradiation dose could fully sterilize wAlbB-SG females. This suggests that Wolbachia-carrying mosquitoes are more sensitive to irradiation, consistent with a previous report showing that a lower irradiation dose fully sterilized Wolbachia-infected Ae. aegypti females (Brazil and Mexican strains) compared to those uninfected controls.
Our findings thus reveal the distinct mechanisms of ionizing X-ray irradiation-induced male or female sterility in Ae. aegypti mosquitoes, which may help the design of X-ray irradiation-based vector control methods.
埃及伊蚊（Aedes aegypti，Ae. aegypti）是传播登革热、寨卡和丝虫病等热带和亚热带地区多种疾病的主要媒介。由于对化学杀虫剂的抗药性不断增强，生物控制方法已成为控制蚊虫种群的新兴方向。不育昆虫技术（SIT）利用高剂量电离辐射对释放前的雄性蚊子进行绝育。基于沃尔巴克氏体的不相容昆虫技术（IIT）的种群抑制方法涉及释放感染沃尔巴克氏体的雄性蚊子，以绝育未感染的野外雌性蚊子。由于缺乏完善的性别分离工具，在雄性种群中检测到低比例的雌性污染。为了防止意外释放这些可能导致种群替代的感染沃尔巴克氏体的雌性蚊子，会使用低剂量 X 射线辐射来绝育任何雌性逃逸者。然而，目前尚不清楚这些辐照诱导的雄性和雌性绝育是否存在共同机制。
在这项工作中，我们着手确定完全绝育埃及伊蚊（NEA-EHI 株）所需的最小剂量 X 射线辐射。进一步的结果表明，这种最小剂量的 X 射线辐射用于雌性绝育会显著降低雄性的生育能力。在之前的几次操作试验中也有类似的报道。通过研究不育的根本原因，我们的研究结果表明，雄性不育可能是由于照射诱导的生殖细胞中的染色体损伤所致。相比之下，雌性不育似乎有所不同，可能是由体细胞支持细胞的消除引起的，这导致了卵原细胞的成熟受阻。在此基础上，我们确定了正在用于 IIT-SIT 现场试验的感染沃尔巴克氏体的 NEA-EHI（wAlbB-SG）菌株的最小剂量 X 射线辐射。与未感染的亲代菌株相比，较低的辐射剂量可以完全绝育 wAlbB-SG 雌性蚊子。这表明携带沃尔巴克氏体的蚊子对辐射更敏感，这与之前的一项研究结果一致，该研究表明，与未感染的对照相比，较低的辐射剂量可完全绝育感染沃尔巴克氏体的埃及伊蚊雌性（巴西和墨西哥株）。
因此，我们的研究结果揭示了埃及伊蚊中电离 X 射线辐射诱导雄性或雌性不育的不同机制，这可能有助于设计基于 X 射线辐射的蚊虫控制方法。
