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Humboldt-Universitaet zu Berlin - Collaborative Research Center for Theoretical Biology

Host manipulation by parasitic endosymbionts: Combining proximate and ultimate approaches

Wolbachia are intracellular bacteria that induce a cytoplasmic mating incompatibility (CI) in many insect species. At the proximate level, this phenomenon is intriguing because the bacteria implement it as a modification-rescue system. That is, if an egg is fertilized by Wolbachia-modified sperm, then Wolbachia must be present in this egg to ensure regular embryonic development. Otherwise, CI manifests itself in irregularities during the first cleavage mitosis that typically lead to embryonic death. We aim to design a mechanistic model of the bacterial strategies underlying these irregularities. The model will be based on recent cytological studies of Wolbachia-induced CI with special focus on the gonomeric spindle and other particularities of the first cleavage mitosis in insects. We seek to elucidate the role of checkpoints and developmental control architecture in the evolution of bacterial host manipulations, paying special attention to targets in cell cycle regulation, such as the spindle assembly checkpoint. We hypothesize that the need for developmental robustness with regard to internal perturbations opens the door for external perturbance by certain parasitic agents. This will help to address the ultimate question why Wolbachia are highly persistent as parasitic endosymbionts of insects on an evolutionary time scale.

CI is similarly intriguing at the ultimate level due to its potential catalyzing effect on host speciation. We aim to examine theoretically a recent field example from Drosophila recens and D. subquinaria where a unilateral Wolbachia-infection seems to have shaped female mating preferences, thereby reinforcing incipient speciation. In addition to suffering from CI, hybrids also face nuclear genetic incompatibilities, as typically found in speciation studies. Our study will thus focus on the potentially synergistic interplay of nuclear and cytoplasmic mating incompatibilities. We expect to show that such synergies can significantly contribute to Wolbachia’s impact on insect speciation and diversity, especially since our previous work estimates the percentage of Wolbachia-infected insect species to be of the order of 60 percent. Leading back to the mechanistic basis of CI, the field example raises a proximate issue: Transfection experiments demonstrate the conversion of Wolbachia-induced syndromes from CI SFB 618 C1 Hammerstein 295 to another phenomenon called male killing. Our efforts to model the mechanism of CI will include an attempt to explain this radical difference in syndromes caused by the same strain of bacteria in different host backgrounds.

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