Evolutionary Ecology ofWolbachiaReleases for Disease Control

Abstract

Wolbachia is an endosymbiotic Alphaproteobacteria that can suppress insect-borne diseases through decreasing host virus transmission (population replacement) or through decreasing host population density (population suppression). We contrast natural Wolbachia infections in insect populations with Wolbachia transinfections in mosquitoes to gain insights into factors potentially affecting the long-term success of Wolbachia releases. Natural Wolbachia infections can spread rapidly, whereas the slow spread of transinfections is governed by deleterious effects on host fitness and demographic factors. Cytoplasmic incompatibility (CI) generated by Wolbachia is central to both population replacement and suppression programs, but CI in nature can be variable and evolve, as can Wolbachia fitness effects and virus blocking. Wolbachia spread is also influenced by environmental factors that decrease Wolbachia titer and reduce maternal Wolbachia transmission frequency. More information is needed on the interactions between Wolbachia and host nuclear/mitochondrial genomes, the interaction between invasion success and local ecological factors, and the long-term stability of Wolbachia-mediated virus blocking.

An elusive endosymbiont: DoesWolbachiaoccur naturally inAedes aegypti?

“…aegypti and Ae. albopictus (Ross et al, 2019b). Most of these infections induce cytoplasmic incompatibility and many also reduce the ability of their hosts to transmit viruses, making them desirable for field release.…”

“…Until recently, Ae. aegypti was not thought to harbor Wolbachia naturally (Kittayapong et al, 2000), though it is clearly amenable to infection given the number of stable experimental infections generated in this species (Ross et al, 2019b). Evidence for horizontal gene transfer between Wolbachia and Ae.…”

“…When novel and natural infections are compatible with each other (no reduction in egg hatch in any combination), invasion will depend on the relative fitness of each infection type due to a lack of cytoplasmic incompatibility ( Figure 1B). Since transinfections in mosquitoes typically impose fitness costs while natural infections tend to be beneficial (Ross et al, 2019b), population replacement may be unachievable even if high frequencies are reached.…”

Persistent deleterious effects of an unstable deleteriousWolbachiainfection

“…Replacement releases can be effective because the presence of Wolbachia in mosquitoes reduces transmission of arboviruses (Moreira et al 2009a;Walker et al 2011;Ant et al 2018). In addition, Wolbachia decreases the fitness of its mosquito hosts (Ross et al 2019c). While this might have a suppressive effect on dengue transmission, for instance, by shortening mosquito lifespan (Cook et al 2008), it can make the infections more difficult to introduce into populations because the initial Wolbachia frequency has to be higher for the population to be invaded by Wolbachia (Hoffmann and Turelli 1997).…”

Does membrane feeding compromise the quality ofAedes aegyptimosquitoes?

“…Other programs involve releases of both males and females which aim to replace natural populations with mosquitoes that have a reduced capacity to transmit diseases. Aedes mosquitoes with Wolbachia infections that block dengue transmission have now been released in several countries [5], while gene drives have recently been developed in Anopheles mosquitoes for both population replacement [6, 7] and suppression [8].…”