Wolbachia’s Deleterious Impact on Aedes aegypti Egg Development: The Potential Role of Nutritional Parasitism

Abstract

The artificial introduction of the endosymbiotic bacterium, Wolbachia pipientis, into Aedes (Ae.) aegypti mosquitoes reduces the ability of mosquitoes to transmit human pathogenic viruses and is now being developed as a biocontrol tool. Successful introgression of Wolbachia-carrying Ae. aegypti into native mosquito populations at field sites in Australia, Indonesia and Malaysia has been associated with reduced disease prevalence in the treated community. In separate field programs, Wolbachia is also being used as a mosquito population suppression tool, where the release of male only Wolbachia-infected Ae. aegypti prevents the native mosquito population from producing viable eggs, subsequently suppressing the wild population. While these technologies show great promise, they require mass rearing of mosquitoes for implementation on a scale that has not previously been done. In addition, Wolbachia induces some negative fitness effects on Ae. aegypti. While these fitness effects differ depending on the Wolbachia strain present, one of the most consistent and significant impacts is the shortened longevity and viability of eggs. This review examines the body of evidence behind Wolbachia’s negative effect on eggs, assesses nutritional parasitism as a key cause and considers how these impacts could be overcome to achieve efficient large-scale rearing of these mosquitoes.

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

“…Dissection of w AlbB-infected females that failed to lay eggs showed that all females were inseminated but lacked mature eggs in their abdomens despite being blood fed. Previous studies suggest that w AlbB has only a minor negative impact on egg viability during the first two months of storage [43]. However, these costs may be underestimated because a high proportion of females hatching from stored eggs are infertile.…”

“…Wolbachia infections compete with their hosts for key nutrients required for egg production [44] which may be exacerbated when female parents are stored as eggs. Egg provisioning or hormone modulation may also be impacted by Wolbachia under stress [43, 45], but this requires further investigation.…”

Designing Effective <em>Wolbachia</em> Release Programs for Mosquito and Arbovirus Control

“…Most drastic are their effects on female fertility, with almost all Wolbachia transinfections reducing fecundity or egg hatch (Axford et al, 2016, Fraser et al, 2017, Ant et al, 2018. These negative effects become pronounced with age, such as when eggs are quiescent (Allman et al, 2020), or appear under poor nutritional conditions (Caragata et al, 2014). Consequently, the negative effects of Wolbachia strains are likely to be underestimated when evaluated under standard laboratory conditions.…”

“…When costs are triggered by environmental conditions, such as high temperatures or low rainfall, releases of Wolbachia-infected mosquitoes can be timed to facilitate the spread of Wolbachia when costs are low, followed by seasonal suppression when costs are high (Rašić et al, 2014. Most Wolbachia transinfections in mosquitoes reduce the viability of quiescent eggs (Allman et al, 2020), making it possible use these strains for population suppression during long dry seasons when rainfall is infrequent. Aedes aegypti carrying the wMel strain of Wolbachia become partially selfincompatible at high temperatures (Ross et al, 2019b), which may decrease population sizes during the hottest times of the year.…”

“…This approach was recently used for Wolbachia replacement releases in the Pacific Islands (http://www.eliminatedengue.com/pi/Progress/view/news/1063/pg/1). However, because storage and transport can reduce Wolbachia-infected egg viability (Allman et al, 2020), remote mass-rearing may increase production requirements and produce lower quality mosquitoes. Controlling mosquito populations by releasing even more mosquitoes may seem counter-intuitive, especially when biting female mosquitoes are released.…”