Factory Tsetse Flies Must Behave Like Wild Flies: A Prerequisite for the Sterile Insect Technique

Tsetse flies are the vectors of human and animal African trypanosomoses, the former a major neglected disease, and the latter considered among the greatest constraints to livestock production in sub-Saharan Africa. To date, the disease is mainly contained through the prophylactic and curative treatment of livestock with trypanocidal drugs, which is not sustainable. The removal of the vector, the tsetse fly, would be the most efficient way of managing these diseases. A number of efficient tsetse control tactics are available that can be combined and applied following areawide integrated pest management (AWIPM) principles [1]. The concept entails (1) the integration of various control tactics, preferably combining those methods that are effective at high population densities with those that are effective at low population densities to obtain maximal efficiency, and (2) the control effort is directed against an entire tsetse population within a delimited area. This is particularly relevant in case eradication is the strategy of choice. Genetic control tactics such as the sterile insect technique (SIT) show great potential for integration in such AW-IPM programmes because they are very efficient for controlling low-density populations, which is not the case for most other techniques. Sterile male insects are reared and, after sterilization with ionizing radiation, sequentially released in large quantities to outnumber the wild male flies. A mating of a sterile male with a virgin wild female fly results in no offspring. Recently, transgenic and paratransgenic techniques have been proposed to sterilize male insects or to make strains refractory to disease parasites in the case of vectors [2–4]. However, to ensure the success of these control methods, factory-reared tsetse flies must be competitive with their wild counterparts and must exhibit a similar behaviour in a natural environment. The SIT as part of an AW-IPM approach is a robust technique, which has proven to be very efficient in eradicating, suppressing, or containing dipteran pests such as Cochliomyia hominivorax (New World screwworm) in Central America, Mexico, the United States, and Libya [5,6], Ceratitis capitata (Mediterranean fruit fly) in Argentina, Chile, Israel, Mexico, Peru, Spain, and the US, Bactrocera cucurbitae (melon fly) in the Okinawa archipelago of Japan, and lepidopteran pests such as Cydia pomonella (codling moth) in Canada, Australian painted apple moth (Teia anartoides) in New Zealand, and Cactoblastic cactorum (cactus moth) and Pectinophora gossypiella (pink bollworm) in Mexico and the US [1]. Similarly, the SIT has been successfully integrated with other control tactics against several tsetse species, i.e., with aerial spraying of insecticides against Glossina morsitans morsitans in Tanzania, with insecticide-impregnated targets and traps against Glossina palpalis gambiensis and Glossina tachinoides in Burkina Faso and G. palpalis palpalis in Nigeria, and with the live-bait technique against Glossina austeni on Unguja Island (Zanzibar). These programmes showed that the SIT against tsetse is feasible, but with the exception of the programme on Unguja Island [7], they proved to be unsustainable. Some have thus questioned whether competitive sterile male tsetse flies can be produced [8], especially since learning mechanisms like site[9] or host-fidelity [10] might influence their behaviour and prevent them from feeding efficiently on wild hosts after being reared on artificial membranes in a laboratory environment. Understanding all the factors that contributed to the success on Unguja Island would be useful for future eradication programmes. Earlier work has already demonstrated that laboratory reared and released sterile tsetse flies were able to feed on wild hosts: (1) recaptured sterile male flies often had residues of blood meals in their digestive tract, (2) a mean lifespan in nature of 11– 17 days [9], which was similar to captured, marked, and released wild males [11], and (3) released sterile male tsetse that received too low a dose of isomethamidium chloride in their blood meal before release were found infected with trypanosomes after release in a natural environment [12], which would have been impossible in the absence of a blood meal on wild hosts. Adequate survival, dispersal, dispersion, mobility, and mating compatibility are critical factors influencing sexual competitiveness of the released sterile male flies [13]. An analysis of the data collected during the AW-IPM programme against G. austeni on the Island of Unguja indicated that the sterile males did not disperse randomly but showed the same spatial distribution as their wild counterparts. The most detailed data sets were available from the primary Jozani Forest Reserve (now part of the Jozani-Chwaka Bay National Park) (6u159S and 39u259E), where the vegetation was very homogeneous and where .300 sterile male flies were released per week per km. All sterile male flies were marked with fluorescent dye, irradiated with 120 Gy, packaged in carton release containers, and released by air at an altitude of 250 m. The release of the sterile male flies by air ensured their random distribution on the island. The release cartons were dropped at very regular intervals and opened upon contact with the airstream that forced the flies out