Distinct spermiogenic phenotypes underlie sperm elimination in theSegregation Distortermeiotic drive system

Abstract

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.

Y chromosome shredding inAnopheles gambiae: insight into the cellular dynamics of a novel synthetic sex ratio distorter

“…Recently, sperm elimination in the presence of a segregation distorter meiotic drive has been investigated in D. melanogaster. In this scenario, the severity of spermatogenic defects is linked to the copy number of the meiotic drive target, the Responder (Rsp) satellite, and in the presence of a high copy number of Rsp, checkpoints are activated during the histone-to-protamine transition, leading to cell death (64). TUNEL assays to investigate if the apoptotic pathway is activated in the Y shredder strains could be conducted in the future (67).…”

Red queen’s race: rapid evolutionary dynamics of an expanding family of meiotic drive factors and their hpRNA suppressors

“…Since sex chromosome conflict is most apparent in the male germline, the homology of Dox family proteins to protamine provides a testable foundation for understanding their role in meiotic drive systems that distort fidelity and quality of spermatogenesis, namely Winters and Durham drive (Tao et al, 2001;Tao et al, 2007b). Interestingly, the most wellknown meiotic drive system in flies, the autosomal Segregation Distorter (SD) system of D. melanogaster (Larracuente and Presgraves, 2012), was recently linked to protamine dysfunction (Herbette et al, 2021), and protamine knockdown also enhances SD drive capacity (Gingell and McLean, 2020). We note that while the histone-to-protamine transition can occur in D. simulans nmy mutants (Yasuno et al, 2013), the stronger condition of D. simulans RNAi mutants (which compromise all hpRNAs) strictly block this process since histones remain associated with dcr-2 and ago2 mutant spermatids (Lin et al, 2018).…”