Infection with Wolbachia protects mosquitoes against Plasmodium‐induced mortality in a natural system

Abstract

In recent years, there has been a shift in the one host‐one parasite paradigm with the realization that, in the field, most hosts are coinfected with multiple parasites. Coinfections are particularly relevant when the host is a vector of diseases, because multiple infections can have drastic consequences for parasite transmission at both the ecological and evolutionary timescales. Wolbachia pipientis is the most common parasitic microorganism in insects, and as such, it is of special interest for understanding the role of coinfections in the outcome of parasite infections. Here, we investigate whether Wolbachia can modulate the effect of Plasmodium on what is, arguably, the most important component of the vectorial capacity of mosquitoes: their longevity. For this purpose, and in contrast to recent studies that have focused on mosquito–Plasmodium and/or mosquito–Wolbachia combinations not found in nature, we work on a Wolbachia–mosquito–Plasmodium triad with a common evolutionary history. Our results show that Wolbachia protects mosquitoes from Plasmodium‐induced mortality. The results are consistent across two different strains of Wolbachia and repeatable across two different experimental blocks. To our knowledge, this is the first time that such an effect has been shown for Plasmodium‐infected mosquitoes and, in particular, in a natural Wolbachia–host combination. We discuss different mechanistic and evolutionary explanations for these results as well as their consequences for Plasmodium transmission.

Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti

“…Some of these associations produced pathogen interference, however for w AlbB infections of Anopheles gambiae , Plasmodium berghei infection was enhanced [31]. This enhancement may be temperature dependent [32], and has also been observed for some native Wolbachia infections, including in Culex pipiens where Wolbachia protects the host against Plasmodium -induced mortality, but also increases susceptibility to infection [33–35]. Interestingly, such enhancement has never been observed for Plasmodium species that infect humans, or in a mosquito with a stable Wolbachia transinfection.…”

Wolbachia Can Enhance Plasmodium Infection in Mosquitoes: Implications for Malaria Control?

“…The type of association within the host is depicted by symbols (target: natural infection, square: stable artificial infection, diamond: transient artificial infection). Numbers indicate: (1) the phenotype is temperature sensitive, (2) Wolbachia infection also increases insect life span [31], which has implications for pathogen transmission. Phylogeny was reconstructed based on work from Carlton et al [26] and Martinsen et al [27].…”

“…Recent studies carried out in Culex pipiens mosquitoes, which are naturally infected with the w Pip Wolbachia strain and transmit the avian malaria parasite P. relictum , have also demonstrated Plasmodium enhancement. In this natural system, Wolbachia protects the mosquito host against the detrimental fitness effects incurred by Plasmodium infection [31] and increases the susceptibility of C. pipiens to P. relictum , with w Pip-infected mosquitoes having a higher prevalence of Plasmodium sporozoites in the salivary glands [16]. These studies show that the Plasmodium -inhibiting properties of Wolbachia are far from universal; certain mosquito– Wolbachia – Plasmodium combinations and experimental conditions transform Wolbachia -infected mosquitoes into better vectors of malaria parasites.…”

“…Although challenging, understanding the evolutionary consequences of novel Wolbachia associations on pathogen transmission and identifying the mechanisms behind Wolbachia modulation of Plasmodium is critical for developing effective control strategies and assessing their long-term feasibility. Insights from non-Anopheline systems where Wolbachia naturally infects the vector may be useful in this regard [16], [31], [39].…”

Analysis of the causes of spawning of large-scale, severe malarial epidemics and their rapid total extinction in western Provence, historically a highly endemic region of France (1745–1850)

“…Wolbachia are intracellular and endosymbiotic bacteria that infect approximately two-thirds of insect species along with numerous other arthropods. Moreover, they are potent modulators of pathogen infection, and although Anopheles mosquitoes are naturally uninfected with these bacteria, artificial infections have shown that Wolbachia strains reduce the level of P. falciparum, although in contrast, a Wolbachia strain enhances oocyst density of P. berghei , the model murine malaria species [251-253]. Infection with Wolbachia can protect mosquitoes against Plasmodium -induced mortality in a natural system [253].…”