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.
Highlights
In sexually reproducing organisms, the production of haploid gametes from diploid germ cells ensures that two alleles of the same locus are transmitted to the progeny
Both alleles of the same gene have an equal chance to be transmitted to the progeny
In many species including mammals, insects and plants, selfish genetic elements perturb gametogenesis in a way that favors their own transmission to the detriment of the homologous chromosome that does not carry them
Summary
The production of haploid gametes from diploid germ cells ensures that two alleles of the same locus are transmitted to the progeny. "meiotic drivers" are widespread across plants, animals and fungi, male-specific meiotic drive systems are well studied in Drosophila species, where 19 independent distorters are currently known [1,2] While most of these drive systems are sex-linked and distort sex ratios, one of the most famous male-specific meiotic drivers is an autosomal selfish gene complex called Segregation Distorter (SD) in D. melanogaster [3,4]. SD is by far the best studied and documented system and belongs to the second category It was first described in 1959 after the discovery of second chromosomes (called SD chromosomes) that induced distortion of the expected Mendelian ratio [3]: in the appropriate genetic background, heterozygous SD/SD+ males transmit the SD chromosome to 95–100% of their progenies
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