Open AccessDistinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system
Author(s) -
Marion Herbette,
Xiaolu Wei,
Ching-Ho Chang,
Amanda M. Larracuente,
Benjamin Loppin,
Raphaëlle Dubruille
Publication year - 2021
Publication title -
plos genetics
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 3.587
H-Index - 233
eISSN - 1553-7404
pISSN - 1553-7390
DOI - 10.1371/journal.pgen.1009662
Subject(s) - biology , spermatid , meiotic drive , genetics , sperm , spermiogenesis , protamine , meiosis , chromatin , microbiology and biotechnology , gene , heparin , biochemistry
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 post-meiotic 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.