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Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila
E A McGraw1, D J Merritt, J N Droller
1Section of Vector Biology, Department of Epidemiology and Public Health, Yale University School of Medicine, 60 College Street, New Haven, CT 06520, USA.
Abstract:
Estimates of Wolbachia density in the eggs, testes and whole flies of drosophilid hosts have been unable to predict the lack of cytoplasmic incompatibility (CI) expression in so-called mod(-) variants. Consequently, the working hypothesis has been that CI expression, although related to Wolbachia density, is also governed by unknown factors that are influenced by both host and bacterial genomes. Here, we compare the behaviour of the mod(-) 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(-) 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-specific control over Wolbachia tissue tropism, and (iv) infection of sperm bundles by the mod(-) D. simulans wCof strain indicates that there are several independent routes by which a strain can be a CI non-expressor.
Insights
The mod(-) Wolbachia popcorn strain fails to induce cytoplasmic incompatibility (CI) in Drosophila melanogaster by not infecting sperm bundles. However, it expresses CI in Drosophila simulans, revealing host-specific control over bacterial tissue tropism.
Area of Science:
- Microbiology
- Genetics
- Evolutionary Biology
Background:
- Cytoplasmic incompatibility (CI) is a form of reproductive manipulation mediated by Wolbachia bacteria.
- Previous studies could not link Wolbachia density to the lack of CI in mod(-) variants, suggesting other genetic factors are involved.
- The mod(-) popcorn strain of Wolbachia in Drosophila melanogaster is a known non-inducer of CI.
Purpose of the Study:
- To investigate the reasons behind the lack of CI expression in the mod(-) popcorn Wolbachia strain.
- To compare the behavior of the popcorn strain in its native host (Drosophila melanogaster) versus a novel host (Drosophila simulans).
- To understand the role of host-bacterial interactions in CI expression and Wolbachia tissue tropism.
Main Methods:
- Comparative analysis of Wolbachia popcorn strain in Drosophila melanogaster and Drosophila simulans.
- Examination of Wolbachia colonization of sperm bundles in both host species.
- Assessment of CI expression in transinfected flies.
Main Results:
- The popcorn strain is genetically similar to other Wolbachia strains found in Drosophila melanogaster.
- The mod(-) phenotype in Drosophila melanogaster is due to the popcorn strain's failure to colonize sperm bundles.
- In Drosophila simulans, the popcorn strain successfully colonizes sperm bundles and induces strong CI, indicating the bacteria possess the necessary genetic machinery.
- Host species significantly influences Wolbachia tissue tropism and CI expression.
Conclusions:
- The mod(-) status of the popcorn strain in Drosophila melanogaster is host-dependent, related to its inability to infect sperm.
- Wolbachia's ability to induce CI is influenced by host-specific factors controlling tissue tropism.
- Multiple independent mechanisms can lead to a Wolbachia strain being a CI non-expressor.