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

Abstract

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.

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

“…The strength of cytoplasmic incompatibly is also related to the density of Wolbachia inside the mosquito, which can be influenced by environmental conditions. The wMel strain in Aedes aegypti shows complete cytoplasmic incompatibility under standard laboratory conditions but weakens when mosquitoes experience high temperatures (Ross et al, 2017) or hatch from quiescent eggs (Lau et al, 2021). For some natural Wolbachia infections, cytoplasmic incompatibility weakens as males age, likely corresponding to a decline in Wolbachia density (Kittayapong et al, 2002).…”

“…aegypti in Malaysia decreased the size of the Ae. aegypti population in some locations (Nazni et al, 2019), possibly due to host fitness costs in mosquitoes hatching from quiescent eggs (Lau et al, 2021). Because all Wolbachia strains being used for population replacement have host fitness costs, observed decreases in dengue transmission could in part be explained by decreased vector population sizes.…”

“…Host fitness costs when eggs are quiescent could be utilized for seasonal population suppression (Lau et al, 2021).…”

“…wAlbB-infected females hatching from quiescent eggs become infertile. This fitness cost could reduce Wolbachia invasion and persistence in locations with long dry seasons (Lau et al, 2021).…”

“…aegypti (Xi et al, 2005) and is similar to wMel in many ways; both strains induce complete cytoplasmic incompatibility and have similar effects on pathogen blocking (Joubert et al, 2016. However, wAlbB is relatively stable at high temperatures (Ross et al, 2017, Ant et al, 2018 and its effects on host fitness can differ to wMel under some environmental conditions (Lau et al, 2021, Lau et al, 2020. When wAlbB-infected Ae.…”