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Wolbachia distribution and cytoplasmic incompatibility during sperm development: the cyst as the basic cellular unit
Michael E Clark1, Zoe Veneti, Kostas Bourtzis
1Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA.
Abstract:
The growth and distribution of the intracellular microbe Wolbachia pipientis during spermatogenesis in several different host/symbiont genetic combinations in Drosophila melanogaster and Drosophila simulans is described. Considerable intra- and inter-strain variation in Wolbachia density and tissue distribution was observed. Wolbachia were found inside spermatocytes and spermatids or within the somatic cyst cells surrounding the germ cells. Some strains displayed both tissue distributions. High rates of cytoplasmic incompatibility (CI) are correlated with high levels of Wolbachia only when spermatocytes and/or spermatids harbor the microbe. Wolbachia infection of somatic cyst cells, although sometimes present at high levels, did not result in significant CI expression. CI-inducing Wolbachia strains within D. simulans showed no distinguishable differences in distribution or density within infected spermatids. To dissect the relative contribution of host and symbiont to the expression of CI, Wolbachia from various host strains known to exhibit varying levels of CI were introgressed into new uninfected host genetic backgrounds. These introgression experiments confirm that the mod(+)/mod(-) phenotype is an intrinsic Wolbachia trait and is not determined by host factors. The level of sperm modification in those lines harboring Wolbachia capable of modifying sperm, however, is influenced by host genetic background. These results form the basis of the Wolbachia Infected Spermatocyte/Spermatid Hypothesis (WISSH). According to WISSH, Wolbachia infection in spermatocytes and then spermatids during sperm development is required for CI expression.
Insights
Wolbachia bacteria in Drosophila sperm cells, specifically spermatocytes and spermatids, are essential for causing cytoplasmic incompatibility (CI). Infection in surrounding somatic cells does not significantly impact CI.
Area of Science:
- Microbiology
- Genetics
- Reproductive Biology
Background:
- Wolbachia pipientis is an intracellular microbe that manipulates insect reproduction.
- Cytoplasmic incompatibility (CI) is a form of reproductive manipulation mediated by Wolbachia.
Purpose of the Study:
- To investigate the distribution and density of Wolbachia during spermatogenesis in Drosophila.
- To determine the correlation between Wolbachia location and CI expression.
- To elucidate the roles of host and symbiont in CI.
Main Methods:
- Microscopic analysis of Wolbachia distribution in Drosophila spermatogenesis.
- Genetic introgression experiments to assess host vs. symbiont contributions to CI.
Main Results:
- Wolbachia density and distribution varied significantly between strains and within tissues.
- High CI rates correlated with Wolbachia presence in spermatocytes and spermatids, not somatic cyst cells.
- The CI-inducing phenotype is an intrinsic Wolbachia trait, but host genetics influence sperm modification levels.
Conclusions:
- Wolbachia infection within spermatocytes and spermatids is necessary for CI expression (Wolbachia Infected Spermatocyte/Spermatid Hypothesis - WISSH).
- Host genetic background modulates the extent of sperm modification by CI-inducing Wolbachia.