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

N. W. Beebe, D. Pagendam, B. J. Trewin, A. Boomer, M. Bradford, A. Ford, C. Liddington, A. Bondarenco, P. J. De Barro, J. Gilchrist, C. Paton, K. M. Staunton, B. Johnson, A. J. Maynard, G. J. Devine, L. E. Hugo, G. Rasic, H. Cook, P. Massaro, N. Snoad, J., Proceedings of the National Academy of Sciences, 118:e2106828118. 2021.

With over 40% of humans at risk from mosquito-borne diseases such as dengue, yellow fever, chikungunya, and Zika, the development of environmentally friendly mosquito-control tools is critical. The release of reproductively incompatible male mosquitoes carrying a Wolbachia bacterium can drive mating events that kill the eggs. Through replicated treatment and control experiments in northern Australia, regular releases of Aedes aegypti males infected with a Wolbachia from Aedes albopictus was shown to drive strong population suppression in mosaic populations of wild-type (no Wolbachia) and wMel-Wolbachia–carrying Ae. aegypti. In a demonstration of bidirectional incompatibility between different Wolbachia strains in the field, we also demonstrate that one season’s suppression experiment can also show an ongoing effect into the following season.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.Field collection data for this IIT experiment has been deposited in a publicly accessible database:Beebe, Nigel (2021): Debug Innisfail data portal version 1. CSIRO. Data collection (https://doi.org/10.25919/3ehh-3q96).