title: Elimination of Y chromosome-bearing spermatids during spermiogenesis in an autosomal sex-ratio mutant of Drosophila simulans.
abstract: Sex ratio distortion, which is commonly abbreviated as sex-ratio, has been studied in many Drosophila species, but the mechanism remains largely unknown. Here, we report on the sex-ratio mutant of D. simulans named excess of females (exf). The third chromosomal recessive mutation results in a sex ratio of approximately 0.2 or less (males/total). Cytological observation demonstrated that meiosis appeared to be completed normally, but that most Y chromosome-bearing nuclei failed to elongate during spermiogenesis, as revealed by fluorescence in situ hybridization using sex chromosome-specific probes. These aberrant nuclei contained membranous inclusions as revealed by electron microscopic analysis. Most of the aberrant exf spermatids failed to individualize and mature, suggesting that a later stage of spermiogenesis is involved in prevention of production of sperm with abnormal morphology. On the one hand, in exf seminal vesicles, sperm nuclei with a length of 5-8.5 μm were occasionally observed, in addition to those with wild-type sperm dimensions, that is, a length of approximately 10 μm. Thus, spermatids with less severe nuclear defects can escape elimination and be released into the seminal vesicles as mature sperm. Furthermore, we constructed His2AvD-GFP and ProtamineB-eGFP transgenic lines in D. simulans, and examined the processes involved in replacement of chromatin proteins over a time course, according to nuclear morphology. We found that both normal and abnormal sperm heads demonstrated equal chromatin replacement during late spermiogenesis. Our results suggest that exf belongs to a unique class of meiotic drive systems in that (1) intranuclear membranous inclusions cause failure of nuclear shaping of Y-bearing spermatids without affecting the histone-protamine transition, and (2) a portion of the aberrant spermatids differentiate into mature sperm; these are transferred to and stored by females.
authors.affiliation: Drosophila Genetic Resource Center, Kyoto Institute of Technology, Saga-Ippongi-cho, Ukyo-ku, Kyoto 616-8354, Japan. yasuno@dgrc.kit.ac.jp
authors.forename: Yusaku
authors.initials: Y
authors.lastname: Yasuno
authors.forename: Yoshihiro H
authors.initials: YH
authors.lastname: Inoue
authors.forename: Masa-Toshi
authors.initials: MT
authors.lastname: Yamamoto
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified / Q000235:genetics / Q000254:growth & development; D002467:Cell Nucleus / Q000235:genetics; D002843:Chromatin / Q000235:genetics; D004330:Drosophila / Q000235:genetics* / Q000254:growth & development; D005260:Female; D005808:Genes, Recessive; D017404:In Situ Hybridization, Fluorescence; D008297:Male; D008540:Meiosis; D046529:Microscopy, Electron, Transmission; D009154:Mutation / Q000235:genetics*; D012730:Sex Chromosomes / Q000235:genetics*; D012744:Sex Ratio; D013087:Spermatids / Q000473:pathology* / Q000648:ultrastructure; D013091:Spermatogenesis / Q000502:physiology*; D014998:Y Chromosome / Q000235:genetics*
chemical_list: D002843:Chromatin