Ecological dynamics of field Aedes albopictus populations under Wolbachia-mediated suppression.

Background: The incompatible insect technique (IIT), based on Wolbachia-induced conditional sterility, has proven highly effective in suppressing mosquito populations for dengue control. However, concerns that accidental release of infected females could drive population replacement have prompted integration of IIT with irradiation or advanced sex-separation technologies. Moreover, the broader ecological consequences of IIT-based suppression remain insufficiently understood. Here, we investigated whether standalone IIT, leveraging Wolbachia-associated fitness costs under real-world conditions, can effectively suppress Aedes albopictus populations without causing replacement, while also addressing key ecological concerns related to IIT-based mosquito population suppression.

Methods: We conducted field trials on Shazai Island, Nansha District, Guangzhou, China, releasing approximately 16,000 Wolbachia wPip-transinfected A. albopictus HC males per hectare per week from 2018 to 2019, following three years of combined IIT and sterile insect technique (SIT) application. Population suppression was monitored, with wPip infection frequency assessed to evaluate population replacement risks. Two-dimensional system of ordinary differential equations incorporating Wolbachia-induced fitness costs was established to predict population dynamics. Additionally, we assessed female mating preferences after three years of suppression and the impact on non-target Culex quinquefasciatus populations.

Results: We offer both empirical evidence and a mathematical model, demonstrating that the fitness costs associated with a Wolbachia triple-strain infection in A. albopictus, especially in adverse field conditions, empower a standalone IIT to effectively suppress mosquito populations without causing population replacement. Remarkably, reducing the previous release numbers to just 20% sustained a similar suppression level. We found no evidence of changes in female mating preferences after a three-year field suppression. The suppression of A. albopictus does not impact the population of the coexisting nontarget species C. quinquefasciatus. After stopping releases, the population rebounded partially in Year 1 and appeared to fully recover in Year 2, with the rate of this recovery likely influenced by mosquito immigration associated with population flow.

Conclusions: Our study demonstrates the robustness, cost-effectiveness, scalability, and ecological safety of IIT as a tool for controlling mosquito-borne diseases. These findings support the implementation of field-applicable, low-dose IIT for sustainable dengue control.