Wolbachia protects Drosophila melanogaster against two naturally occurring and virulent viral pathogens

Abstract

Wolbachia is a common endosymbiont that can protect insects against viral pathogens. However, whether the antiviral effects of Wolbachia have a significant effect on fitness remains unclear. We have investigated the interaction between Drosophila melanogaster, Wolbachia and two viruses that we recently isolated from wild flies, La Jolla virus (LJV; Iflaviridae) and Newfield virus (NFV; Permutotetraviridae). Flies infected with these viruses have increased mortality rates, and NFV partially sterilizes females. These effects on fitness were reduced in Wolbachia-infected flies, and this was associated with reduced viral titres. However, Wolbachia alone also reduces survival, and under our experimental conditions these costs of the symbiont can outweigh the benefits of antiviral protection. In contrast, protection against the sterilizing effect of NFV leads to a net benefit of Wolbachia infection after exposure to the virus. These results support the hypothesis that Wolbachia is an important defense against the natural pathogens of D. melanogaster. Furthermore, by reducing the cost of Wolbachia infection, the antiviral effects of Wolbachia may aid its invasion into populations and help explain why it is so common in nature.

Figure 1

The effect of Wolbachia on viral titre. (A) Viral titre in flies with and without Wolbachia that were inoculated with LJV or NFV. The line is a three-parameter asymptotic exponential growth curve, the shaded areas are 95% confidence intervals, and each point is an RNA extraction from 10 flies. (B) Viral titre 10 days post oral infection with NFV. Each point represents the virus titre of a single fly. The square is the mean and error bars 95% bootstrap confidence interval. Viral titres were estimated by quantitative PCR relative to the concentration of RpL32 mRNA. Virus was detected in all samples. Male flies were added 3–5 days post eclosion.

Figure 2

The effect of virus and Wolbachia infection on mortality. Shaded area is the 95% confidence interval. Each line is estimated from 307 to 383 flies. Male flies were infected 3–5 days post eclosion.

Figure 3

The effect of virus and Wolbachia infection on female fecundity. Egg production in flies with and without Wolbachia that had been (A) inoculated with LJV or NFV or (B) fed NFV. Each dot represents the number of eggs laid per single female over 24 h. The bars are means, and error bars 95% confidence intervals. Flies were infected 3–5 days post eclosion.