Wolbachiadensity and virulence attenuation after transfer into a novel host

Abstract

The factors that control replication rate of the intracellular bacterium Wolbachia pipientis in its insect hosts are unknown and difficult to explore, given the complex interaction of symbiont and host genotypes. Using a strain of Wolbachia that is known to over-replicate and shorten the lifespan of its Drosophila melanogaster host, we have tracked the evolution of replication control in both somatic and reproductive tissues in a novel host͞Wolbachia association. After transinfection (the transfer of a Wolbachia strain into a different species) of the over-replicating Wolbachia popcorn strain from D. melanogaster to Drosophila simulans, we demonstrated that initial high densities in the ovaries were in excess of what was required for perfect maternal transmission, and were likely causing reductions in reproductive fitness. Both densities and fitness costs associated with ovary infection rapidly declined in the generations after transinfection. The early death effect in D. simulans attenuated only slightly and was comparable to that induced in D. melanogaster. This study reveals a strong host involvement in Wolbachia replication rates, the independence of density control responses in different tissues, and the strength of natural selection acting on reproductive fitness. W olbachia pipientis are common bacterial endosymbionts of arthropods and filarial nematodes. They occur intracellularly in the ovaries of all described hosts, as well as in a number of other tissues depending on the particular Wolbachia͞host combination (1, 2). Infection of the host germ line enables transovarial transmission as well as induction of a number of reproductive abnormalities. These include cytoplasmic incompatibility (CI), parthenogenesis, feminization, and male killing, all of which enhance the spread of Wolbachia in host populations (3).In Drosophila simulans and Drosophila melanogaster, most infections induce CI (4), where Wolbachia modify developing sperm such that only the presence of the same Wolbachia strain in the egg can rescue the modification, allowing successful completion of karyogamy (5, 6) and the subsequent normal development of the embryo. Uninfected females cannot rescue the sperm modification, and so the development of their offspring is blocked. The result is that with each subsequent generation, infection frequencies rise and fewer and fewer uninfected females can successfully reproduce (7).For infections to be maintained in host populations, Wolbachia replication rates must be sufficiently high to ensure fidelity of transovarial transmission, while being low enough to not cause overt host pathology. This replication control can be considered a defining feature that separates vertically transmitted symbionts from horizontally transmitted pathogens. The mechanisms that underlie control of Wolbachia replication and the extent to which this control is influenced by host or bacterial genotype are not well understood. Studies exploring the link between CI expression and Wolbachia infection densities have revealed tha...

WolbachiastrainwMel induces cytoplasmic incompatibility and blocks dengue transmission inAedes albopictus

“…1). A similar effect was previously reported in newly transinfected Drosophila (22) and Ae. aegypti (6).…”

The evolution of endosymbiont density in doubly infected host species

“…This assumption is corroborated by a number of studies on the bacterium Wolbachia. For example, it has been demonstrated that after transinfection of the Wolbachia strain popcorn from its native host Drosophila melanogaster to D. simulans, decrease of bacterial numbers in the ovaries over nine generations corresponded to increased fecundity of infected females (McGraw et al, 2002). The assumption is also supported by the observation that among the two CI-inducing Wolbachia strains that infect the mosquito Aedes albopictus, the one with the higher transmission rate is also the one with the higher bacterial density Dutton & Sinkins, 2004).…”

Toward a Wolbachia Multilocus Sequence Typing System: Discrimination of Wolbachia Strains Present in Drosophila Species

“…Based on our data these strains clearly share a common ancestor, share identical wsp sequences [61], but can be discriminated by sampling dnaA and pdhB. All three strains are known to be CIinducers [9,24,36,37], and the wMelPop strain has also been shown to reduce the life span of its hosts, D.…”