B chromosomes reveal a female meiotic drive suppression system in Drosophila melanogaster

Selfish genetic elements use a myriad of mechanisms to drive their inheritance and ensure their survival into the next generation, often at a fitness cost to its host.1,2 Although the catalog of selfish genetic elements is rapidly growing, our understanding of host drive suppression systems that counteract self-seeking behavior is lacking. Here, we demonstrate that the biased transmission of the non-essential, non-driving B chromo-somes in Drosophila melanogaster can be achieved in a specific genetic background. Combining a null mutant of matrimony, a gene that encodes a female-specific meiotic regulator of Polo kinase,3,4 with the TM3 balancer chromosome creates a driving genotype that is permissive for the biased transmission of the B chromosomes. This drive is female-specific, and both genetic components are necessary, but not indi-vidually sufficient, for permitting a strong drive of the B chromosomes. Examination of metaphase I oocytes reveals that B chromosome localization within the DNA mass is mostly abnormal when drive is the strongest, indicating a failure of the mechanism(s) responsible for the proper distribution of B chromosomes. We pro-pose that some proteins important for proper chromosome segregation during meiosis, like Matrimony, may have an essential role as part of a meiotic drive suppression system that modulates chromosome segregation to prevent genetic elements from exploiting the inherent asymmetry of female meiosis.

Automated summary

Selfish genetic elements use various mechanisms to ensure their inheritance and survival at the expense of the host. However, our understanding of the suppression systems against such selfish behavior is limited. In this study, the biased transmission of non-essential B chromosomes in Drosophila melanogaster was achieved in a specific genetic background. The combination of a mutant of the matrimony gene and the TM3 balancer chromosome created a female-specific driving genotype for the biased transmission of the B chromosomes. The abnormal localization of B chromosomes during meiosis suggests a failure in the mechanism responsible for their proper distribution.