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Comparative Study
. 2017 May 30;15(5):e2001894.
doi: 10.1371/journal.pbio.2001894. eCollection 2017 May.

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

Tom L Schmidt  1 , Nicholas H Barton  2 , Gordana Rašić  1 , Andrew P Turley  3 , Brian L Montgomery  3 , Inaki Iturbe-Ormaetxe  3 , Peter E Cook  3 , Peter A Ryan  3 , Scott A Ritchie  4 , Ary A Hoffmann  1 , Scott L O'Neill  3 , Michael Turelli  5
Affiliations
Comparative Study

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

Tom L Schmidt et al. PLoS Biol. .

Abstract

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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Release zone locations in Cairns.
The 3 release areas are Edge Hill/Whitfield (EHW), Parramatta Park (PP), and Westcourt (WC). Locations of the 2 major highways, Mulgrave Road and Captain Cook Highway, are indicated in light blue and red, respectively. Locations of onsite traps (traps within the release zones) are plotted as black dots within white circles, and offsite traps (outside the release zones) are plotted as white circles. (The underlying road network is derived from "Australia Oceania Continent Roads," made available by MapCruzin.com and OpenStreetMap.org under the Open Database License [https://opendatacommons.org/licenses/odbl/1.0/].)
Fig 2
Fig 2. Average trap captures for infected and uninfected Ae. aegypti.
Ae. aegypti caught offsite (A) and onsite (B) are graphed atop weekly Cairns rainfall. Yields and rainfall are smoothed using a moving average of the 5 most recent observations. Trap yields are plotted on a logarithmic scale to show comparative rates of change. After accounting for the seasonal trend in abundances, uninfected mosquito yields offsite (A) decreased over time at both Parramatta Park (PP) and Edge Hill/Whitfield (EHW). Offsite yields of infected mosquitoes increased at PP towards the end of the study but remained relatively constant at EHW. Onsite (B) yields of infected mosquitoes remained relatively constant at EHW and PP, while uninfected mosquito yields decreased heavily in the second dry season (D2) but recovered in the following season.
Fig 3
Fig 3. Ordinary Kriging of infection frequency (p) among traps at Edge Hill/Whitfield (EHW).
Kriging (spatial averaging) was performed using an exponential semivariogram model and a 24-point, nearest-neighbour search function for the first dry season (D1) (panel A), the first wet season (W1) (B), the second dry season (D2) (C), and the second wet season (W2) (D). The central black polygon depicts the release zone. Trap locations are plotted as circles atop each Kriging map and are sized by a logarithmic function of the trap yield from each season. To the left of each Kriging plot, a stacked column chart displays the areas enclosed by the p > 0.8 and p > 0.5 contours. Although a contraction took place in D2, the area increased in W2, despite infection frequency decreasing in several sites within the release zone.
Fig 4
Fig 4. Ordinary Kriging of infection frequency (p) among traps at Parramatta Park (PP).
Kriging was performed as in Fig 3 for the first dry season (D1) (A), the first wet season (W1) (B), the second dry season (D2) (C), and the second wet season (W2). The central black polygon depicts the release zone. Trap locations are plotted as circles atop each Kriging map and are sized by a logarithmic function of the trap yield from each season. To the left of each Kriging plot, a stacked column chart displays the areas enclosed by the p > 0.8 and p > 0.5 contours, showing a constant increase in the invaded area over time.
Fig 5
Fig 5. Ordinary Kriging of infection frequency (p) among traps at Westcourt (WC).
Kriging was performed using an exponential semivariogram model and a 16-point nearest-neighbour search function for the first dry season (D1) (A), the first wet season (W1) (B), the second dry season (D2) (C), and the second wet season (W2). The central black polygon depicts the release zone. Trap locations are plotted as circles atop each Kriging map and are sized by a logarithmic function of the trap yield from each season. To the left of each Kriging plot, a stacked column chart displays the areas enclosed by the p > 0.8 and p > 0.5 contours, showing a decline in the area of infection following W1.
Fig 6
Fig 6. Estimating rates of spatial spread and wave width for Edge Hill/Whitfield (EHW) and Parramatta Park (PP).
Panels A and B plot the estimates of r0 and w (from S2 Table) through time for EHW; panels C and D show the estimates for PP. The x axis in each panel represents days; the releases began on day 99 and ended on day 197. The slopes of the fitted regression lines imply wave speeds of cd = 0.474 m per day at EHW and cd = 0.289 m per day at PP. See the text for discussion and interpretation.
Fig 7
Fig 7. Likelihood analysis of the Westcourt (WC) data.
Panels A and B plot the estimates of r0 and w (from S6 Table) through time for WC. See the text for discussion and interpretation.
Fig 8
Fig 8. The statistical Model (7) describing the position and width of the wave.
Assuming wave width w = 1, the figure illustrates the transition from a near-Gaussian distribution of infection frequencies near the centre of the release (for r0 = 0.25, 0.5) to a wave traveling in both directions (for r0 = 1, 2, 4, 8).
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References

    1. Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol. 2002;10: 100–3. - PubMed
    1. Guzman A, Istúriz RE. Update on the global spread of dengue. Int J Antimicrob Agents. 2010;36: S40–2. - PubMed
    1. Bogoch II, Brady OJ, Kraemer M, German M, Creatore MI, Kulkarni MA, et al. Anticipating the international spread of Zika virus from Brazil. Lancet. 2016;387: 335–6. 10.1016/S0140-6736(16)00080-5 - DOI - PMC - PubMed
    1. Weaver SC, Lecuit M. Chikungunya virus and the global spread of a mosquito-borne disease. N Engl J Med. 2015;372: 1231–9. 10.1056/NEJMra1406035 - DOI - PubMed
    1. McGraw EA, O'Neill SL. Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol. 2013;11: 181–93. 10.1038/nrmicro2968 - DOI - PubMed

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