Reduced competence to arboviruses following the sustainable invasion of<i>Wolbachia</i>into native<i>Aedes aegypti</i>from Niterói, Southeastern Brazil

Gesto, João Silveira Moledo; Ribeiro, Gabriel Sylvestre; Rocha, Marcele Neves; Peixoto, Julia; Carvalho, Fabiano Duarte; Pereira, Thiago Nunes; Moreira, Luciano Andrade

doi:10.1101/2020.09.25.312207

Cited by 8 publications

(9 citation statements)

References 64 publications

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“…Error bars represent means ± standard errors. https://doi.org/10.1371/journal.pntd.0009179.g005 PLOS NEGLECTED TROPICAL DISEASES programs because they do not require local mass-rearing facilities [13,16,42] and allow eggs to be accumulated across several weeks before being transported for release. Although most releases to date have involved the wMel strain, wAlbB was used for releases in Malaysia [16] based on its desirable characteristic of being stable in its density and phenotypic effects under high temperatures [43].…”

Section: Discussionmentioning

confidence: 99%

Infertility and fecundity loss of Wolbachia-infected Aedes aegypti hatched from quiescent eggs is expected to alter invasion dynamics

2021

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The endosymbiotic bacterium Wolbachia shows viral blocking in its mosquito host, leading to its use in arboviral disease control. Releases with Wolbachia strains wMel and wAlbB infecting Aedes aegypti have taken place in several countries. Mosquito egg survival is a key factor influencing population persistence and this trait is also important when eggs are stored prior to releases. We therefore tested the viability of mosquitoes derived from Wolbachia wMel and wAlbB-infected as well as uninfected eggs after long-term storage under diurnal temperature cycles of 11–19°C and 22–30°C. Eggs stored at 11–19°C had higher hatch proportions than those stored at 22–30°C. Adult Wolbachia density declined when they emerged from eggs stored for longer, which was associated with incomplete cytoplasmic incompatibility (CI) when wMel-infected males were crossed with uninfected females. Females from stored eggs at both temperatures continued to show perfect maternal transmission of Wolbachia, but storage reduced the fecundity of both wMel and wAlbB-infected females relative to uninfected mosquitoes. Furthermore, we found a very strong negative impact of the wAlbB infection on the fertility of females stored at 22–30°C, with almost 80% of females hatching after 11 weeks of storage being infertile. Our findings provide guidance for storing Wolbachia-infected A. aegypti eggs to ensure high fitness adult mosquitoes for release. Importantly, they also highlight the likely impact of egg quiescence on the population dynamics of Wolbachia-infected populations in the field, and the potential for Wolbachia to suppress mosquito populations through cumulative fitness costs across warm and dry periods, with expected effects on dengue transmission.

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Section: Discussionmentioning

confidence: 99%

Infertility and fecundity loss of Wolbachia-infected Aedes aegypti hatched from quiescent eggs is expected to alter invasion dynamics

2021

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“…These releases can involve adults or eggs. Releases involving eggs, where containers of eggs are hatched directly in the field, are desirable for Wolbachia release programs because they do not require local mass-rearing facilities [13,16,41] and allow eggs to be accumulated across several weeks before being transported for release. Although most releases to date have involved the wMel strain, wAlbB was used for releases in Malaysia [16] based on its desirable characteristic of being stable in its density and phenotypic effects under high temperatures [42].…”

Section: Discussionmentioning

confidence: 99%

Infertility and fecundity loss ofWolbachia-infectedAedes aegyptihatched from quiescent eggs is expected to alter invasion dynamics

Lau

Ross

Hoffmann

2020

Preprint

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The endosymbiotic bacterium Wolbachia shows viral blockage in its mosquito host, leading to its use in arboviral disease control. Releases with Wolbachia strains wMel and wAlbB infecting Aedes aegypti have taken place in several countries. Mosquito egg survival is a key factor influencing population persistence and this trait is also important when eggs are stored prior to releases. We therefore tested the viability of mosquitoes derived from Wolbachia wMel and wAlbB-infected as well as uninfected eggs after long-term storage under diurnal temperature cycles of 11-19°C and 22-30°C. Eggs stored at 11-19°C had higher hatch proportions than those stored at 22-30°C. Adult Wolbachia density declined when they emerged from eggs stored for longer, which was associated with incomplete cytoplasmic incompatibility (CI) when wMel-infected males were crossed with uninfected females. wAlbB-infected males continued to show complete CI. Females from stored eggs at both temperatures continued to show perfect maternal transmission of Wolbachia, but storage reduced the fecundity of both wMel and wAlbB-infected females relative to uninfected mosquitoes. Furthermore, we found a very strong negative impact of the wAlbB infection on the fertility of females stored at 22-30°C, with almost 80% of females hatching after 11 weeks of storage being infertile. Our findings provide guidance for storing Wolbachia-infected Ae. aegypti eggs to ensure high fitness adult mosquitoes for release. Importantly, they also highlight the likely impact of egg quiescence on the population dynamics of Wolbachia-infected populations in the field, and the potential for Wolbachia to suppress mosquito populations through cumulative fitness costs across warm and dry periods, with expected effects on dengue transmission.

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“…Releases of wMel-infected Ae. aegypti have now been carried out in several dengue-endemic cities including Yogyakarta, Indonesia [18] and Rio de Janeiro [19,20] and Niterói [21,22], Brazil. Quasiexperimental and/or randomized controlled trials show that wMel releases have reduced dengue incidence by >69% [8,22,23], with reductions in chikungunya and Zika transmission also apparent in some locations [22].…”

Section: Introductionmentioning

confidence: 99%

A decade of stability for wMel Wolbachia in natural Aedes aegypti populations

Ross

Robinson

Yang

et al. 2021

Preprint

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Mosquitoes carrying Wolbachia endosymbionts are being released in many countries for arbovirus control. The wMel strain of Wolbachia blocks Aedes-borne virus transmission and can spread throughout mosquito populations by inducing cytoplasmic incompatibility. Aedes aegypti mosquitoes carrying wMel were first released into the field in Cairns, Australia, over a decade ago, and with wider releases have resulted in the near elimination of local dengue transmission. The long-term stability of Wolbachia effects is critical for ongoing disease suppression, requiring tracking of phenotypic and genomic changes in Wolbachia infections following releases. We used a combination of field surveys, phenotypic assessments, and Wolbachia genome sequencing to show that wMel has remained stable in its effects for up to a decade in Australian Ae. aegypti populations. Phenotypic comparisons of wMel-infected and uninfected mosquitoes from near-field and long-term laboratory populations suggest limited changes in the effects of wMel on mosquito fitness. Treating mosquitoes with antibiotics used to cure the wMel infection had limited effects on fitness in the next generation, supporting the use of tetracycline for generating uninfected mosquitoes without off-target effects. wMel has a temporally stable within-host density and continues to induce complete cytoplasmic incompatibility. A comparison of wMel genomes from pre-release (2010) and nine years post-release (2020) populations show few genomic differences and little divergence between release locations, consistent with the lack of phenotypic changes. These results indicate that releases of Wolbachia-infected mosquitoes for population replacement are likely to be effective for many years, but ongoing monitoring remains important to track potential evolutionary changes.Author summaryWolbachia are endosymbionts that can block the transmission of arboviruses by mosquitoes. Aedes aegypti mosquitoes carrying the wMel strain of Wolbachia have been released in ‘population replacement’ interventions, which aim to establish wMel in mosquito populations, thereby reducing their ability to spread disease. Wolbachia population replacement programs began only a decade ago, raising uncertainty about their long-term effectiveness. Here we provide a comprehensive assessment of the long-term stability of wMel from the very first Wolbachia population replacement release. We show that there is no evidence for changes in the phenotypic effects of wMel in mosquitoes, and confirm that the wMel genome has changed very little in the decade since field releases began. wMel remains at high levels within mosquitoes, suggesting that its ability to block virus transmission has been retained. Our data provides confidence that Wolbachia population replacement releases will provide ongoing protection against arbovirus transmission.

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Reduced competence to arboviruses following the sustainable invasion ofWolbachiainto nativeAedes aegyptifrom Niterói, Southeastern Brazil

Cited by 8 publications

References 64 publications

Infertility and fecundity loss of Wolbachia-infected Aedes aegypti hatched from quiescent eggs is expected to alter invasion dynamics

Infertility and fecundity loss of Wolbachia-infected Aedes aegypti hatched from quiescent eggs is expected to alter invasion dynamics

Infertility and fecundity loss ofWolbachia-infectedAedes aegyptihatched from quiescent eggs is expected to alter invasion dynamics

A decade of stability for wMel Wolbachia in natural Aedes aegypti populations

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