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

Tom L. Schmidt, Nicholas H. Barton, Gordana Rašić, Andrew P. Turley, Brian L. Montgomery, Inaki Iturbe-Ormaetxe, Peter E. Cook, Peter A. Ryan, Scott A. Ritchie, Ary A. Hoffmann, Scott L. O’Neill, Michael Turelli

Research output: Contribution to journalArticleResearchpeer-review

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 km2and 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.

Original languageEnglish
Article numbere2001894
Number of pages28
JournalPLoS Biology
Volume15
Issue number5
DOIs
Publication statusPublished - 30 May 2017

Cite this

Schmidt, T. L., Barton, N. H., Rašić, G., Turley, A. P., Montgomery, B. L., Iturbe-Ormaetxe, I., ... Turelli, M. (2017). Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. PLoS Biology, 15(5), [e2001894]. https://doi.org/10.1371/journal.pbio.2001894
Schmidt, Tom L. ; Barton, Nicholas H. ; Rašić, Gordana ; Turley, Andrew P. ; Montgomery, Brian L. ; Iturbe-Ormaetxe, Inaki ; Cook, Peter E. ; Ryan, Peter A. ; Ritchie, Scott A. ; Hoffmann, Ary A. ; O’Neill, Scott L. ; Turelli, Michael. / Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. In: PLoS Biology. 2017 ; Vol. 15, No. 5.
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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 km2and 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 = "Schmidt, {Tom L.} and Barton, {Nicholas H.} and Gordana Rašić and Turley, {Andrew P.} and Montgomery, {Brian L.} and Inaki Iturbe-Ormaetxe and Cook, {Peter E.} and Ryan, {Peter A.} and Ritchie, {Scott A.} and Hoffmann, {Ary A.} and O’Neill, {Scott L.} and Michael Turelli",
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Schmidt, TL, Barton, NH, Rašić, G, Turley, AP, Montgomery, BL, Iturbe-Ormaetxe, I, Cook, PE, Ryan, PA, Ritchie, SA, Hoffmann, AA, O’Neill, SL & Turelli, M 2017, 'Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti' PLoS Biology, vol. 15, no. 5, e2001894. https://doi.org/10.1371/journal.pbio.2001894

Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. / Schmidt, Tom L.; Barton, Nicholas H.; Rašić, Gordana; Turley, Andrew P.; Montgomery, Brian L.; Iturbe-Ormaetxe, Inaki; Cook, Peter E.; Ryan, Peter A.; Ritchie, Scott A.; Hoffmann, Ary A.; O’Neill, Scott L.; Turelli, Michael.

In: PLoS Biology, Vol. 15, No. 5, e2001894, 30.05.2017.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti

AU - Schmidt, Tom L.

AU - Barton, Nicholas H.

AU - Rašić, Gordana

AU - Turley, Andrew P.

AU - Montgomery, Brian L.

AU - Iturbe-Ormaetxe, Inaki

AU - Cook, Peter E.

AU - Ryan, Peter A.

AU - Ritchie, Scott A.

AU - Hoffmann, Ary A.

AU - O’Neill, Scott L.

AU - Turelli, Michael

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N2 - 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 km2and 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.

AB - 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 km2and 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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