Wolbachia bacterium sterilises male insects, preventing reproduction

In a first for the Southern Hemisphere, researchers have shown that a bacterium can successfully suppress populations of the invasive, disease-carrying Aedes aegypti mosquito that is responsible for spreading dengue, yellow fever and Zika.

Published in PNAS (see abstract below), the trial involved releasing three million male Aedes aegypti mosquitoes in Northern Queensland, sterilised with a naturally occurring bacterium called Wolbachia, across three trial sites over a 20-week period during the summer of 2018. The sterile male insects search out and mate with wild females, preventing the production of offspring.  

Scientists returned the following year and found one of the trial sites, Mourilyan in Queensland, was almost devoid of mosquitoes.

Risks

This approach to mosquito population reduction does not involve genetically engineered mosquitoes or gene drives, two technologies that are being promoted as solutions to mosquito-borne diseases, despite the evidence of failure.

Although Aedes aegypti is not a native mosquito to Australia, having been introduced from Africa over a hundred years ago, GMWatch cautions that any technology (GM or not) aimed at reducing or eradicating populations of wild species may have unexpected harmful effects that need careful assessment. For example, populations of natural predators that feed on the target species may be threatened, causing a long-term ecological imbalance that could result in a surge in the target species. Also, reducing or eradicating one species that is seen as a pest could create an "ecological niche" for an even more destructive species to move into.

But this Wolbachia approach at least does not add the unpredictable risks of using GM technology, let alone CRISPR gene drives, on top of these more general risks.

Natural alternatives to suppression

Interestingly, there are also ways of using the naturally occurring Wolbachia bacterium only to disrupt the mosquitoes’ ability to transmit viruses, rather than to eliminate the mosquitoes themselves. This is done by releasing females carrying the Wolbachia bacterium.

In one instance, this approach reduced the incidence of dengue in an Australian town to zero over four years following the release of mosquitoes carrying Wolbachia, that then spread the bacterium throughout the wild population during mating. Before the study, the city experienced dengue outbreaks every year.

A more carefully controlled study, conducted in an Indonesian city, showed releasing Wolbachia-infected mosquitoes led to a steep drop (77%) in cases of dengue fever. This randomized, double-blind trial provided such strong evidence for Wolbachia’s effectiveness in tackling mosquito-borne diseases that epidemiologists told the journal Nature that the findings were “staggering” and “epochal”.

And Wolbachia is not the only naturally occurring biocontrol agent that is showing promise. Last year the journal Nature Communications reported on a microbe that inhibits the development of the malaria parasite in the mosquito Anopheles arabiensis, which spreads malaria in Sub-Saharan Africa.

80% of mosquito population suppressed

This latest Wolbachia trial, involving population suppression as a means of stopping viral transmission, was an international collaboration between Australia’s national science agency CSIRO, University of Queensland (UQ), Verily Life Sciences, QIMR Berghofer Medical Research Institute and James Cook University (JCU).  

CSIRO scientist and UQ associate professor, Nigel Beebe, said the trial demonstrates this technique is robust and capable of effectively suppressing mosquito populations.

“During the trial, we saw over 80 per cent of the mosquito population suppressed across our three trial sites,” Prof Beebe said.

“When we surveyed the sites the following year, we were very encouraged to see the suppression still in effect, with one of our most productive towns for Aedes aegypti almost devoid of this mosquito with a 97 per cent reduction across the following season.  

“One year on, the mosquito population at the second trial site remained substantially suppressed, while the population fully recovered at the third site.  

“We are currently investigating the differences observed in the following mosquito season as they are incredibly informative in further developing this technology and in modelling how we could remove this exotic virus-transmitting pest in other locations worldwide.”

The technique can also be used to remove the virus-transmitting Asian tiger mosquito, Aedes albopictus, that has now established at Australia’s doorstep in the Torres Strait Islands.  

Techniques from the trial are being used to support CSIRO-led mosquito suppression programs in French Polynesia and the Hunter region in New South Wales, Australia.
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Releasing incompatible males drives strong suppression across populations of wild and Wolbachia-carrying Aedes aegypti in Australia
Nigel W. Beebe et al (2021). PNAS October 12, 2021 118 (41) e2106828118; https://doi.org/10.1073/pnas.2106828118
https://www.pnas.org/content/118/41/e2106828118

Significance

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.

Abstract

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.

Image of Wolbachia bacterium by Scott O'Neill via Wiki Commons. Reproduced under licence Attribution 2.5 Generic (CC BY 2.5)