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...
Estimates of Wolbachia density in the eggs, testes and whole £ies of drosophilid hosts have been unable to predict the lack of cytoplasmic incompatibility (CI) expression in so-called mod 7 variants. Consequently, the working hypothesis has been that CI expression, although related to Wolbachia density, is also governed by unknown factors that are in£uenced by both host and bacterial genomes. Here, we compare the behaviour of the mod 7 over-replicating Wolbachia popcorn strain in its native Drosophila melanogaster host to the same strain transinfected into a novel host, namely Drosophila simulans. We report that (i) the popcorn strain is a close relative of other D. melanogaster infections, (ii) the mod 7 status of popcorn in D. melanogaster appears to result from its inability to colonize sperm bundles, (iii) popcorn is present in the bundles in D. simulans and induces strong CI expression, which demonstrates that the bacterial strain does not lack the genetic machinery for inducing CI and that there is host-species-speci¢c control over Wolbachia tissue tropism, and (iv) infection of sperm bundles by the mod 7 D. simulans wCof strain indicates that there are several independent routes by which a strain can be a CI non-expressor.
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