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A new model and method for understanding Wolbachia-induced cytoplasmic incompatibility.

Bossan B, Koehncke A, Hammerstein P - PLoS ONE (2011)

Bottom Line: The mistiming-model requires fewer assumptions but has been contradicted by empirical results.Finally, we suggest empirical tests that would allow to distinguish between the models.Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

View Article: PubMed Central - PubMed

Affiliation: Institute for Theoretical Biology, Humboldt University, Berlin, Germany. benjamin.bossan@hu-berlin.de

ABSTRACT
Wolbachia are intracellular bacteria transmitted almost exclusively vertically through eggs. In response to this mode of transmission, Wolbachia strategically manipulate their insect hosts' reproduction. In the most common manipulation type, cytoplasmic incompatibility, infected males can only mate with infected females, but infected females can mate with all males. The mechanism of cytoplasmic incompatibility is unknown; theoretical and empirical findings need to converge to broaden our understanding of this phenomenon. For this purpose, two prominent models have been proposed: the mistiming-model and the lock-key-model. The former states that Wolbachia manipulate sperm of infected males to induce a fatal delay of the male pronucleus during the first embryonic division, but that the bacteria can compensate the delay by slowing down mitosis in fertilized eggs. The latter states that Wolbachia deposit damaging "locks" on sperm DNA of infected males, but can also provide matching "keys" in infected eggs to undo the damage. The lock-key-model, however, needs to assume a large number of locks and keys to explain all existing incompatibility patterns. The mistiming-model requires fewer assumptions but has been contradicted by empirical results. We therefore expand the mistiming-model by one quantitative dimension to create the new, so-called goalkeeper-model. Using a method based on formal logic, we show that both lock-key- and goalkeeper-model are consistent with existing data. Compared to the lock-key-model, however, the goalkeeper-model assumes only two factors and provides an idea of the evolutionary emergence of cytoplasmic incompatibility. Available cytological evidence suggests that the hypothesized second factor of the goalkeeper-model may indeed exist. Finally, we suggest empirical tests that would allow to distinguish between the models. Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

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Related in: MedlinePlus

Explanation of the compatiblity relationship using the goalkeeper-model.The points represent the contribution by the corresponding Wolbachia strain to the two mod factors ( and ). The black arrow represents the host contribution to rescue. The contribution of a strain to the two resc factors equals its own contribution plus the net host contribution. When both resc factors exceed both mod factors in quantity, rescue is successful. Thus wTei with the help of the net host contribution rescues wRi (indicated by wRi being within the dotted frame). In contrast, wRi can rescue wMel but not wTei (indicated by wMel but not wTei being within the dashed frame).
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pone-0019757-g004: Explanation of the compatiblity relationship using the goalkeeper-model.The points represent the contribution by the corresponding Wolbachia strain to the two mod factors ( and ). The black arrow represents the host contribution to rescue. The contribution of a strain to the two resc factors equals its own contribution plus the net host contribution. When both resc factors exceed both mod factors in quantity, rescue is successful. Thus wTei with the help of the net host contribution rescues wRi (indicated by wRi being within the dotted frame). In contrast, wRi can rescue wMel but not wTei (indicated by wMel but not wTei being within the dashed frame).

Mentions: Our analysis shows that the goalkeeper-model can be fitted to many different compatibility relationships despite the model's mere two factors. In the example of the six Wolbachia strains we studied, a possible distribution of the two factors that can explain the data is presented in Fig. 4. This compatibility relationship would not be possible without assuming that the host contributes to the amount of rescue factors (black arrow). To summarize, we could show that the goalkeeper-model can explain the experimentally found compatibility relationships among these six Wolbachia strains.


A new model and method for understanding Wolbachia-induced cytoplasmic incompatibility.

Bossan B, Koehncke A, Hammerstein P - PLoS ONE (2011)

Explanation of the compatiblity relationship using the goalkeeper-model.The points represent the contribution by the corresponding Wolbachia strain to the two mod factors ( and ). The black arrow represents the host contribution to rescue. The contribution of a strain to the two resc factors equals its own contribution plus the net host contribution. When both resc factors exceed both mod factors in quantity, rescue is successful. Thus wTei with the help of the net host contribution rescues wRi (indicated by wRi being within the dotted frame). In contrast, wRi can rescue wMel but not wTei (indicated by wMel but not wTei being within the dashed frame).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3091874&req=5

pone-0019757-g004: Explanation of the compatiblity relationship using the goalkeeper-model.The points represent the contribution by the corresponding Wolbachia strain to the two mod factors ( and ). The black arrow represents the host contribution to rescue. The contribution of a strain to the two resc factors equals its own contribution plus the net host contribution. When both resc factors exceed both mod factors in quantity, rescue is successful. Thus wTei with the help of the net host contribution rescues wRi (indicated by wRi being within the dotted frame). In contrast, wRi can rescue wMel but not wTei (indicated by wMel but not wTei being within the dashed frame).
Mentions: Our analysis shows that the goalkeeper-model can be fitted to many different compatibility relationships despite the model's mere two factors. In the example of the six Wolbachia strains we studied, a possible distribution of the two factors that can explain the data is presented in Fig. 4. This compatibility relationship would not be possible without assuming that the host contributes to the amount of rescue factors (black arrow). To summarize, we could show that the goalkeeper-model can explain the experimentally found compatibility relationships among these six Wolbachia strains.

Bottom Line: The mistiming-model requires fewer assumptions but has been contradicted by empirical results.Finally, we suggest empirical tests that would allow to distinguish between the models.Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

View Article: PubMed Central - PubMed

Affiliation: Institute for Theoretical Biology, Humboldt University, Berlin, Germany. benjamin.bossan@hu-berlin.de

ABSTRACT
Wolbachia are intracellular bacteria transmitted almost exclusively vertically through eggs. In response to this mode of transmission, Wolbachia strategically manipulate their insect hosts' reproduction. In the most common manipulation type, cytoplasmic incompatibility, infected males can only mate with infected females, but infected females can mate with all males. The mechanism of cytoplasmic incompatibility is unknown; theoretical and empirical findings need to converge to broaden our understanding of this phenomenon. For this purpose, two prominent models have been proposed: the mistiming-model and the lock-key-model. The former states that Wolbachia manipulate sperm of infected males to induce a fatal delay of the male pronucleus during the first embryonic division, but that the bacteria can compensate the delay by slowing down mitosis in fertilized eggs. The latter states that Wolbachia deposit damaging "locks" on sperm DNA of infected males, but can also provide matching "keys" in infected eggs to undo the damage. The lock-key-model, however, needs to assume a large number of locks and keys to explain all existing incompatibility patterns. The mistiming-model requires fewer assumptions but has been contradicted by empirical results. We therefore expand the mistiming-model by one quantitative dimension to create the new, so-called goalkeeper-model. Using a method based on formal logic, we show that both lock-key- and goalkeeper-model are consistent with existing data. Compared to the lock-key-model, however, the goalkeeper-model assumes only two factors and provides an idea of the evolutionary emergence of cytoplasmic incompatibility. Available cytological evidence suggests that the hypothesized second factor of the goalkeeper-model may indeed exist. Finally, we suggest empirical tests that would allow to distinguish between the models. Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

Show MeSH
Related in: MedlinePlus