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

Abstract

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.

Local adaptation ofAedes aegyptimosquitoes toWolbachia-induced fitness costs

“…Here we used a combination of repeated field collections, antibiotic curing and reciprocal backcrossing to show that fitness costs depend on genetic background and shift with laboratory adaptation. This finding is consistent with previous studies demonstrating the potential for host genetic changes to mediate fitness costs [15,41] and the lack of changes in the wMel genome itself [21][22][23]. We have previously found that the genomes of Ae.…”

“…In Cairns, Australia, post-release monitoring found persistent costs of the wMel infection to female fertility [26] and sustained virus blocking [40] after one year. Phenotypic effects have largely persisted in the longer term, with one exception being development time where costs were only apparent in a laboratory background [23]. However, no studies to date have identified the basis of population differences.…”

“…Releasing a Wolbachia strain that induces fitness costs is expected to cause evolutionary changes in either the mosquito or Wolbachia to attenuate these effects [19,20]. While the wMel genome has remained unchanged [21][22][23] there is currently a limited understanding mosquito adaptation to Wolbachia infections. The Ae.…”

“…Currently, there is no evidence that wMel fitness costs have shifted much under field conditions [23,26]. There is also no evidence for differences in fitness costs of wMel between mosquito genetic backgrounds that have had long-term coadaptation versus naïve backgrounds [23].…”

“…Currently, there is no evidence that wMel fitness costs have shifted much under field conditions [23,26]. There is also no evidence for differences in fitness costs of wMel between mosquito genetic backgrounds that have had long-term coadaptation versus naïve backgrounds [23]. However, phenotypic comparisons have covered only a limited number of traits, most of which are only minimally influenced by wMel infection, and quiescent egg viability costs have not been compared between backgrounds.…”