Evaluating the biological quality of mass-reared Anopheles arabiensis males irradiated as pupae or as adults

Abstract

Background: The success of a sterile insect technique programme to control target mosquito populations depends on producing high-quality sterile males that can compete with wild males to inseminate wild females, to consequently inhibit procreation. To succeed, the released males require high biological quality. The quality of laboratory-reared, sterile males can be affected by the rearing conditions, handling, transportation, and irradiation. Limiting the cumulative damage caused by all these processes is key to maintain sterile male performance in the field once released. The ideal life stage to irradiate Anopheles arabiensis males is still an important question for this species. This study aims to assess the dose response of irradiated males at pupal versus adult stages and use quality control (QC) parameters to assess the feasibility and possible advantages of shifting to adult irradiation in this species.

Methods: Laboratory reared An. arabiensis males were irradiated as late-stage pupae or as adults at varying doses to compare the radiosensitivity in both developmental stages. Males irradiated at fully sterilizing doses were further subjected to quality control tests to compare the quality of males irradiated at adult versus pupae stages. The QC parameters tested included flight ability, longevity and mating competitiveness.

Results: The results show that adults do not require more radiation dose to achieve the target sterility, and females are more radiosensitive than males. Longevity, flight ability and mating competitiveness were improved significantly in males irradiated as adults compared to that of males irradiated as pupae.

Conclusions: Given the challenges in synchronizing pupation in a mass rearing setting and achieving a homogenous age (i.e. late-stage pupae) of collected pupae in this species, as well as these findings on the overall improvement of sterile male quality in the males irradiated as adults, this report provides a strong argument for irradiation protocols to shift towards adult stage irradiation in SIT programmes against An. arabiensis.

Keywords: Fitness; Life stage; Malaria vector; Quality control; Sterile insect technique.

Fig. 1

Dose response curves. Dose–response curves, fitted with the Gompertz function, for the effect of radiation dose on the sterility rate according to the sex and the life stage. Blue lines show male adult (left panel) and pupae (right panel) dose response, and pink lines show female adult (left panel) and pupae (right panel) dose response

Fig. 2

Male longevity. Survival curves of An. arabiensis males irradiated as pupae and adult, as compared to the non-irradiated males. Males irradiated as pupae (blue dotted line) showed reduced longevity over 2 weeks

Fig. 3

Flight ability. Escape rates of males irradiated at pupal or adult stage, compared to non-irradiated control males. The box plot shows the mean ± SE, and median and upper and lower quartiles

Fig. 4

Mating competitiveness. Hatch rates resulting from mating crosses with males irradiated at adult (A) or pupal (P) stage compared to fertile (Cf) and sterile (Cs) controls. The box plot shows the mean ± SE, and median and upper and lower quartiles. Higher hatch rates in the pupal irradiation treatment group show reduced competitiveness of these males compared to males irradiated as adults treatment group