Cytoplasmic incompatibility management to support Incompatible Insect Technique against Aedes albopictus

Abstract

Background: The transinfection of the endosymbiotic bacterium Wolbachia provides a method to produce functionally sterile males to be used to suppress mosquito vectors. ARwP is a wPip Wolbachia infected Aedes albopictus which exhibits a bidirectional incompatibility pattern with wild-types. We coupled a modelistic approach with laboratory experiments to test ARwP as a control tool and evaluate the possible occurrence of population replacement following the release of ARwP females in a wild-type (S_ANG) population. Repeated male-only releases were simulated and tested in the laboratory in comparison with releases contaminated with 1% ARwP females. Model simulations also investigated how migration affects the outcome of contaminated releases. Finally, the mean level of egg fertility and the long-term evolution of populations constituted by two Wolbachia infection types were studied by testing S_ANG and ARwP Ae. albopictus and performing more general model simulations.

Results: The model was parametrized with laboratory data and simulations were compared with results of biological trials. Small populations of ARwP males and females were theoretically and experimentally demonstrated to rapidly become extinct when released in larger S_ANG populations. Male-only releases at a 5:1 ratio with respect to the wild-type males led to a complete suppression of the S_ANG population in a few generations. Contaminated releases were efficient as well but led to population replacement in the long term, when the wild-type population approached eradication. Migration significantly contrasted this trend as a 5% population turnover was sufficient to avoid any risk of population replacement. At equal frequencies between ARwP and S_ANG individuals, the mean egg fertility of the overall population was more than halved and suppression was self-sustaining until one of the two infection types extinguished.

Conclusions: In the case of bidirectional incompatibility patterns, the repeated release of incompatible males with small percentages of contaminant females could lead to population replacement in confined environments while it could be managed to target high efficiency and sustainability in wild-type suppression when systems are open to migration. This possibility is discussed based on various contexts and taking into consideration the possibility of integration with other control methods such as SIT and the use of larvicides.

Keywords: ARwP; SIT; Wolbachia; bidirectional incompatibility; population replacement; population suppression; risk assessment.

Fig. 1

ARwP is unable to invade a wild-type Ae. albopictus population. The experiment started from from a ratio of 1:5 ARwP:S_ANG individuals and at 1:1 sex ratio. Due to the Bidirectional Incompatibility pattern, a fast decrease in the frequency of the ARwP infection type was observed in the following generations. Experimental data are compared with model predictions which also show a region of space illustrating the female fecundity (m) intrinsic variability. The reduced chi-square was 0.88

Fig. 2

Suppression of a S_ANG Ae. albopictus wild-type population by the IIT_i approach. The IIT_i trials were characterized by the periodical release (a release for generation) of ARwP males at 5:1 ratio with S_ANG males. Under the tested experimental conditions the wild-type population was eradicated in a few generations. Experimental data are compared with model predictions which also show a region of space illustrating the female fecundity (m) intrinsic variability. The reduced chi-square for the IIT_i trials was 1.01

Fig. 3

Suppression of a S_ANG Ae. albopictus wild-type population by the IIT_c approach. The IIT_c trials were characterized by the periodical release (a release for generation) of ARwP individuals at 5:1 ratio with S_ANG males. Male releases were 1% contaminated by ARwP females. Under the tested experimental conditions the wild-type population was rapidly suppressed however, in 1 case out of 5, the ARwP infection type replaced S_ANG and established, leading to the failure of the control strategy. Experimental data are compared with model predictions which also show a region of space illustrating the female fecundity (m) intrinsic variability. The reduced chi-square for the IIT_c trials was 1.04

Fig. 4

Simulation of the effects of migration on Ae. albopictus population dynamics and ARwP spreading when applying an IIT_c approach. The introduction of a factor accounting for the migration of individuals has a profound impact on the outcome of the model simulation of the IIT_c. Increasing the percent population turnover (0, 1, 2, 5%) means gradually delaying the population replacement by ARwP of the wild-type Ae. albopictus population

Fig. 5

Simulation of the population dynamics on varying immature survival (S₀) when incompatible infection types coexist at 1:1 ratio. The model simulation is relative to a mixed Ae. albopictus population constituted by two bidirectionally incompatible Wolbachia infection types at a ratio of 1:1. Mean immature survival for Ae. albopictus in nature is known to approach 20% [58]. Halving egg fertility by introducing bidirectional CI could make the population more susceptible to control measures targeting larval stage. Under the tested conditions, eradication became achievable by reducing immature survival to 10% and without requiring further incompatible male releases. S₀ percent data are reported in legend as proportions

Fig. 6

Simulation of the expected population dynamics when one or two Wolbachia infection types are present. The simulation shows the evolution of two systems subjected, respectively, to IIT_i and IIT_c after stopping incompatible male releases. As IIT_i releases are stopped, the natural population growth rate is suddenly restored. This outcome is common to all of the methods based on the release of sterile males. The IIT_c model simulation started with a mixed Ae. albopictus population constituted by two bidirectionally incompatible Wolbachia infection types at a ratio of 45:55. The control effects of the latter strategy last for several generations as incompatible males continue to be produced until the females of the infection type at lower frequency gradually extinguish