Increased biting rate and decreased Wolbachia density in irradiated Aedes mosquitoes

Abstract

Background Releasing considerable numbers of radiation-sterilized males is a promising strategy to suppress mosquito vectors. However, releases may also include small percentages of biting females, which translate to non-negligible numbers when releases are large. Currently, the effects of irradiation on host-seeking and host-biting behaviors have not been exhaustively investigated. Information is also lacking regarding the effects of sterilizing treatment on the endosymbiotic bacterium Wolbachia, which is known to affect the vector competence of infected mosquitos. Methods To ascertain the effects of irradiation on females, the pupae of two Aedes albopictus strains, differing in their natural or artificial Wolbachia infection type, and Aedes aegypti—which is not infected by Wolbachia—were treated with various doses of X-rays and monitored for key fitness parameters and biting behavior over a period of 2 weeks. The effect of radiation on Wolbachia was investigated by quantitative polymerase chain reaction (qPCR) and fluorescence in situ hybridization (FISH) analysis. Results Partial Aedes albopictus female sterility was achieved at 28 Gy, but the number of weekly bites more than doubled compared to that of the controls. Radiation doses of 35 and 45 Gy completely inhibited progeny production but did not significantly affect the survival or flight ability of Ae. albopictus females and caused a tripling of the number of bites per female per week (compared to untreated controls). These results were also confirmed in Ae. aegypti after treatment at 50 Gy. Wolbachia density decreased significantly in 45-Gy-irradiated females, with the greatest decreases in the early irradiation group (26 ± 2-h-old pupae). Wolbachia density also decreased as adults aged. This trend was confirmed in ovaries but not in extra-ovarian tissues. FISH analysis showed a strongly reduced Wolbachia-specific fluorescence in the ovaries of 13 ± 1-day-old females. Conclusions These results suggest that, under sterile insect technique (SIT) programs, the vector capacity of a target population could increase with the frequency of the irradiated females co-released with the sterile males due to an increased biting rate. In the context of successful suppression, the related safety issues are expected to be generally negligible, but they should be conservatively evaluated when large-scale programs relying on imperfect sexing and high overflooding release ratios are run for long periods in areas endemic for arboviral diseases. Also, the effects of irradiation on the vector competence deserve further investigation. Graphical Abstract

Wolbachiainhibits ovarian formation and increases blood feeding rate in femaleAedes aegypti

“…This behavioural change of Wolbachia -infected infertile females has significant implications for vector control population release strategies [8, 61]; in particular it would be interesting to test whether the ability of these infertile females to carry and transmit arbovirus has changed as the density of their Wolbachia infection may be lower than that of fertile females [62, 63]. Similar concerns have been raised about increased biting frequencies of irradiated female mosquitoes in sterile insect technique programs [64], however the prevalence of infertile females is likely to be much higher in Wolbachia -infected mosquito populations compared to irradiated females that are only released accidentally.…”

Wolbachia inhibits ovarian formation and increases blood feeding rate in female Aedes aegypti

“…to test whether the ability of these infertile females to carry and transmit arbovirus has changed as the density of their Wolbachia infection may be lower than that of fertile females [66,67]. Similar concerns have been raised about increased biting frequencies of irradiated female mosquitoes in sterile insect technique (SIT) programs [68], however in population replacement approaches the prevalence of infertile females is likely to be much higher in Wolbachia-infected mosquito populations compared to in SIT irradiated females that are only released accidentally.…”

Corrigendum: Developing the radiation‐based sterile insect technique (SIT) for controlling Aedes aegypti: identification of a sterilizing dose

“…Considering the contrasting findings between the investigation conducted by Moretti et al 1 . and Chen et al 2 .…”

“…‘Increased biting rate and decreased Wolbachia density in irradiated Aedes mosquitoes,’ Parasites and Vectors 15 :67 (2022). In their study, Moretti et al 1 . show that female Ae.…”

“…We observed blood‐feeding as an ancillary observation to our main study goals because initial observations suggested that fewer irradiated females were feeding. By contrast, Moretti et al 1 . assessed female feeding by offering groups of 5‐day‐old females an anesthetized mouse to feed on, and the number of engorged females was observed over 20 min.…”