Releasing incompatible males drives strong suppression across populations of wild and Wolbachia-carrying Aedes aegypti in Australia

Releasing sterile or incompatible male insects is a proven method of population management in agricultural systems with the potential to revolutionize mosquito control. Through a collaborative venture with the “Debug” Verily Life Sciences team, we assessed the incompatible insect technique (IIT) with the mosquito vector Aedes aegypti in northern Australia in a replicated treatment control field trial. Backcrossing a US strain of Ae. aegypti carrying Wolbachia wAlbB from Aedes albopictus with a local strain, we generated a wAlbB2-F4 strain incompatible with both the wild-type (no Wolbachia) and wMel-Wolbachia Ae. aegypti now extant in North Queensland. The wAlbB2-F4 strain was manually mass reared with males separated from females using Verily sex-sorting technologies to obtain no detectable female contamination in the field. With community consent, we delivered a total of three million IIT males into three isolated landscapes of over 200 houses each, releasing ∼50 males per house three times a week over 20 wk. Detecting initial overflooding ratios of between 5:1 and 10:1, strong population declines well beyond 80% were detected across all treatment landscapes when compared to controls. Monitoring through the following season to observe the ongoing effect saw one treatment landscape devoid of adult Ae. aegypti early in the season. A second landscape showed reduced adults, and the third recovered fully. These encouraging results in suppressing both wild-type and wMel-Ae. aegypti confirms the utility of bidirectional incompatibility in the field setting, show the IIT to be robust, and indicate that the removal of this arbovirus vector from human-occupied landscapes may be achievable.

High Incidence of Related Wolbachia across Unrelated Leaf-Mining Diptera

The maternally inherited endosymbiont, Wolbachia pipientis, plays an important role in the ecology and evolution of many of its hosts by affecting host reproduction and fitness. Here, we investigated 13 dipteran leaf-mining species to characterize Wolbachia infections and the potential for this endosymbiont in biocontrol. Wolbachia infections were present in 12 species, including 10 species where the Wolbachia infection was at or near fixation. A comparison of Wolbachia relatedness based on the wsp/MLST gene set showed that unrelated leaf-mining species often shared similar Wolbachia, suggesting common horizontal transfer. We established a colony of Liriomyza brassicae and found adult Wolbachia density was stable; although Wolbachia density differed between the sexes, with females having a 20-fold higher density than males. Wolbachia density increased during L. brassicae development, with higher densities in pupae than larvae. We removed Wolbachia using tetracycline and performed reciprocal crosses between Wolbachia-infected and uninfected individuals. Cured females crossed with infected males failed to produce offspring, indicating that Wolbachia induced complete cytoplasmic incompatibility in L. brassicae. The results highlight the potential of Wolbachia to suppress Liriomyza pests based on approaches such as the incompatible insect technique, where infected males are released into populations lacking Wolbachia or with a different incompatible infection.

Wolbachia-mediated sterility suppresses Aedes aegypti populations in the urban tropics

Incompatible insect technique (IIT) via releases of male Wolbachia-infected mosquitoes is a promising tool for dengue control. In a three-year trial in Singaporean high-rise housing estates, we demonstrated that Wolbachia-based IIT dramatically reduces both wildtype Aedes aegypti populations [reductions of 92.7% (95% CI: 84.7%-95.8%) and 98.3% (97.7%-99.8%)] and dengue incidence [reductions of 71% (43%-87%) to 88% (57%-99%)] in the targeted areas. The study highlights the need to ensure adequate vertical distribution of released males in high-rise buildings, address immigration of wildtype females from neighboring areas, and prevent and mitigate stable establishment of Wolbachia in field mosquito populations. Our results demonstrate the potential of Wolbachia-based IIT (supplemented with irradiation, in Singapore's context) for strengthening dengue control in tropical cities, where dengue burden is the greatest.

Aedes albopictus bionomics in Procida Island, a promising Mediterranean site for the assessment of innovative and community-based integrated pest management methods

The colonization of Mediterranean Europe and of other temperate regions by Aedes albopictus created in the last decades an unprecedented nuisance problem in highly infested areas, as well as a new public health threat due to the species competence to transmit exotic arboviruses, such as dengue, chikungunya and zika. The Sterile Insect Technique (SIT) and the Incompatible Insect Technique (IIT) are insecticide-free mosquito-control methods relying on mass release of irradiated/manipulated males which are believed to have a potential in complementing existing and only partially effective control tools. Testing and implementing these approaches are challenging and selection of study sites is an instrumental and crucial step. We carried out a 4-year study in Procida Island (Gulf of Naples, Italy) in strict collaboration with local administrators and citizens to estimate: i) the temporal dynamics, spatial distribution, and population size of Ae. albopictus; and ii) the dispersal and survival of irradiated males. Overall, results provide insights on the bionomics of the mosquito in Southern Europe and draw attention to Procida Island as an ideal site to test innovative control programs against Ae. albopictus which may be used in other Mediterranean and temperate areas.”

Modelling the Wolbachia incompatible insect technique: strategies for effective mosquito population elimination

Background The Wolbachia incompatible insect technique (IIT) shows promise as a method for eliminating populations of invasive mosquitoes such as Aedes aegypti (Linnaeus) (Diptera: Culicidae) and reducing the incidence of vector-borne diseases such as dengue, chikungunya and Zika. Successful implementation of this biological control strategy relies on high-fidelity separation of male from female insects in mass production systems for inundative release into landscapes. Processes for sex-separating mosquitoes are typically error-prone and laborious, and IIT programmes run the risk of releasing Wolbachia-infected females and replacing wild mosquito populations. Results We introduce a simple Markov population process model for studying mosquito populations subjected to a Wolbachia-IIT programme which exhibit an unstable equilibrium threshold. The model is used to study, in silico, scenarios that are likely to yield a successful elimination result. Our results suggest that elimination is best achieved by releasing males at rates that adapt to the ever-decreasing wild population, thus reducing the risk of releasing Wolbachia-infected females while reducing costs. Conclusions While very high-fidelity sex separation is required to avoid establishment, release programmes tend to be robust to the release of a small number of Wolbachia-infected females. These findings will inform and enhance the next generation of Wolbachia-IIT population control strategies that are already showing great promise in field trials.

A One-Sided Competition Mathematical Model for the Sterile Insect Technique

We study a simple mathematical model describing the dynamics of a wild-type pest insects population experiencing competition from sterile insects (one-sided competition). This model can be used for conceiving control strategies based on the Sterile Insect Technique (SIT) or the Incompatible Insect Technique (IIT), aiming to reduce or eradicate Red Palm Weevil (RPW) populations in some target regions. We show that suppression may occur for continuous and periodic release strategies for various intraspecific and interspecific submodels except in the case of a single release strategy where a strong Allee effect is required.

Modelling the Wolbachia Incompatible Insect Technique: strategies for effective mosquito population elimination

The Wolbachia Incompatible Insect Technique (IIT) shows promise as a method for eliminating invasive mosquitoes such as Aedes aegypti (Linnaeus)(Diptera: Culicidae) and reducing the incidence of vector-borne diseases such as dengue, chikungunya and Zika. Successful implementation of this biological control strategy relies on high-fidelity separation of male from female insects in mass production systems for inundative release into landscapes. Processes for sex-separating mosquitoes are typically error prone, laborious and IIT programs run the risk of releasing Wolbachia infected females and replacing wild mosquito populations. We introduce a simple Markov Population Process (MPP) model for studying mosquito populations subjected to a Wolbachia-IIT program which exhibit an unstable equilibrium threshold. The model is used to study, in silico, scenarios that are likely to yield a successful elimination result. Our results suggest that elimination is best achieved by releasing males at rates that adapt to the ever-decreasing wild population, thus reducing the risk of releasing Wolbachia-infected females while reducing costs. While very high-fidelity sex-separation is required to avoid establishment, release programs tend to be robust to the release of a small number of Wolbachia-infected females. These findings will inform and enhance the next generation of Wolbachia-IIT control strategies that are already showing great promise in field trials.