Distinct spermiogenic phenotypes underlie sperm elimination in theSegregation Distortermeiotic drive system

Segregation Distorter(SD) is a male meiotic drive system inDrosophila melanogaster.Males heterozygous for a selfishSDchromosome rarely transmit the homologousSD⁺chromosome. It is well established that distortion results from an interaction betweenSd, the primary distorting locus on theSDchromosome and its target, a satellite DNA calledRsp,on theSD⁺chromosome. However, the molecular and cellular mechanisms leading to post-meioticSD⁺sperm elimination remain unclear. Here we show thatSD/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 otherSD/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 differentSD⁺chromosomes suggest that the severity of the spermiogenic defects associates with the copy number of theRspsatellite. We propose that whenRspcopy 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.