Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system

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Herbette, Marion | Wei, Xiaolu | Chang, Ching-Ho | Larracuente, Amanda | Loppin, Benjamin | Dubruille, Raphaëlle

Edité par CCSD ; Public Library of Science -

International audience. Segregation Distorter (SD) is a male meiotic drive system in Drosophila melanogaster. Males heterozygous for a selfish SD chromosome rarely transmit the homologous SD + chromosome. It is well established that distortion results from an interaction between Sd, the primary distorting locus on the SD chromosome and its target, a satellite DNA called Rsp, on the SD + chromosome. However, the molecular and cellular mechanisms leading to postmeiotic SD + sperm elimination remain unclear. Here we show that SD/SD + males of different genotypes but with similarly strong degrees of distortion have distinct spermiogenic phenotypes. In some genotypes, SD + spermatids fail to fully incorporate protamines after the removal of histones, and degenerate during the individualization stage of spermiogenesis. In contrast, in other SD/SD + genotypes, protamine incorporation appears less disturbed, yet spermatid nuclei are abnormally compacted, and mature sperm nuclei are eventually released in the seminal vesicle. Our analyses of different SD + chromosomes suggest that the severity of the spermiogenic defects associates with the copy number of the Rsp satellite. We propose that when Rsp copy number is very high (> 2000), spermatid nuclear compaction defects reach a threshold that triggers a checkpoint controlling sperm chromatin quality to eliminate abnormal spermatids during individualization.

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