A cascade of destabilizations: combining Wolbachia and Allee effects to eradicate the insect pest Drosophila suzukii. – CrashPest

The dramatic increase in problems caused by invasive species worldwide, paralleled by the planned abandonment of chemical pesticides, makes the development of sustainable pest management strategies a top research priority. The CrashPest project aims at developing a novel, environmentally-friendly method to control insect pests, based on the sole use of intrinsic population processes: an optimal combination of Wolbachia-induced cytoplasmic incompatibility and Allee effects triggered by mating failures. The maternally-transmitted intracellular bacteria Wolbachia have attracted attention for their potential as biocontrol agents. These symbionts are naturally present in many insects and often induce cytoplasmic incompatibility, a form of conditional sterility: infected males produce no offspring unless they mate with a female infected with the same bacterial strain. Maternal transmission and reproductive advantage of infected females yields a crucial property: any Wolbachia strain occurring above a threshold frequency should progressively invade the host population. From this, recent mathematical models have predicted that the successful inoculation of incompatible strains in a target pest population should produce a temporary increase in the frequency of incompatible matings and, in turn, a transient decrease in pest abundance. When combined with mating disruption the pest population could, in theory, reduce to an Allee threshold and decline to extinction.
The CrashPest project will test the efficiency of this strategy on an emerging agricultural pest: Drosophila suzukii. Armed with a highly sclerotized ovipositor, females lay eggs in a wide variety of healthy fruits. Since its invasion of Europe and America, this species has become a major burden of the fruit industry, with economic losses reaching millions of dollars annually. Methods to control natural populations in the field mainly rely on the use of chemical pesticides, but broad-spectrum treatments used are not fully effective and are progressively restricted. Classical biological control approaches based on natural enemies might be challenging because this species has a remarkable resistance to larval parasitoids. Control of this new pest is thus a real scientific and technical challenge.
The project is based on a multidisciplinary approach combining theory and experiments. It is subdivided into four tasks in which different organization levels will be considered. Through the development and analysis of mathematical models, theoretical predictions of the effectiveness of Wolbachia in controlling D. suzukii will be made (Task 1). Behavioural experiments will be performed at the individual level (Task 2) to determine how social, environmental (component Allee effect, sexual confusion) and internal (Wolbachia infection) factors interact and may change the direction, strength and form of sexual selection. In Task 3 the model predictions obtained in task 1 will be tested in population cages by following the effects (separately and combined) of Wolbachia and intrinsic demographic processes on the host populations dynamics. The final task (Task 4) will use parameters determined in the three other tasks to test the efficiency of the combined use of Wolbachia and Allee effect to control D. suzukii populations in a complex environment (mesocosm).
This project will provide novel research avenues as-well as mid-term applications on the use of cytoplasmic incompatibility and Allee effects to eradicate insect pests, and more generally, on the use of intrinsic destabilizing processes as a novel strategy to doom unwanted populations to extinction. Results will thus have both fundamental and applied output.