Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti

Dengue-suppressing Wolbachia strains are promising tools for arbovirus control, particularly as they have the potential to self-spread following local introductions. To test this, we followed the frequency of the transinfected Wolbachia strain wMel through Ae. aegypti in Cairns, Australia, following releases at 3 nonisolated locations within the city in early 2013. Spatial spread was analysed graphically using interpolation and by fitting a statistical model describing the position and width of the wave. For the larger 2 of the 3 releases (covering 0.97 km2 and 0.52 km2), we observed slow but steady spatial spread, at about 100–200 m per year, roughly consistent with theoretical predictions. In contrast, the smallest release (0.11 km2) produced erratic temporal and spatial dynamics, with little evidence of spread after 2 years. This is consistent with the prediction concerning fitness-decreasing Wolbachia transinfections that a minimum release area is needed to achieve stable local establishment and spread in continuous habitats. Our graphical and likelihood analyses produced broadly consistent estimates of wave speed and wave width. Spread at all sites was spatially heterogeneous, suggesting that environmental heterogeneity will affect large-scale Wolbachia transformations of urban mosquito populations. The persistence and spread of Wolbachia in release areas meeting minimum area requirements indicates the promise of successful large-scale population transformation.Author summary: Wolbachia are bacteria that live inside insect cells. In insects that act as viral vectors, Wolbachia can suppress virus transmission to new hosts. Wolbachia have been experimentally introduced into Aedes aegypti mosquito populations to reduce the transmission of dengue, Zika, and other arboviruses that cause human disease. Wolbachia invade populations by causing cytoplasmic incompatibility, a phenomenon whereby embryos from crosses between infected males and uninfected females fail to hatch. While Wolbachia have been shown to successfully invade and remain established in isolated Ae. aegypti populations, outward spread from urban release zones has not been previously documented. This is an important step in demonstrating that Wolbachia can be used to combat mosquito-borne infectious disease in cities. Here we describe Wolbachia spread from 2 introduction areas within Cairns in northeastern Australia at a rate of about 100–200 meters per year. Spread occurs only when introduction areas are sufficiently large. The slow rates of observed spread are broadly consistent with mathematical predictions based on estimated Ae. aegypti dispersal distances, Wolbachia dynamics, and effects seen in isolated populations. Spread is uneven and likely depends on local characteristics (e.g., barriers) that affect mosquito density and dispersal. Our data indicate that Wolbachia can be introduced locally in large cities, remain established where released, and slowly spread from release areas. These dynamics indicate that high Wolbachia infection frequencies can be established gradually across large urban areas through local releases.