In most sexually reproducing organisms, the fundamental process of meiosis is implemented concurrently with two differentiation programs that occur at different rates and generate distinct cell types, sperm and oocytes. However, little is known about how the meiotic program is influenced by such contrasting developmental programs. Here we present a detailed timeline of late meiotic prophase during spermatogenesis in Caenorhabditis elegans using cytological and molecular landmarks to interrelate changes in chromosome dynamics with germ cell cellularization, spindle formation, and cell cycle transitions. This analysis expands our understanding C. elegans spermatogenesis, as it identifies multiple spermatogenesis-specific features of the meiotic program and provides a framework for comparative studies. Post-pachytene chromatin of spermatocytes is distinct from that of oocytes in both composition and morphology. Strikingly, C. elegans spermatogenesis includes a previously undescribed karyosome stage, a common but poorly understood feature of meiosis in many organisms. We find that karyosome formation, in which chromosomes form a constricted mass within an intact nuclear envelope, follows desynapsis, involves a global down-regulation of transcription, and may support the sequential activation of multiple kinases that prepare spermatocytes for meiotic divisions. In spermatocytes, the presence of centrioles alters both the relative timing of meiotic spindle assembly and its ultimate structure. These microtubule differences are accompanied by differences in kinetochores, which connect microtubules to chromosomes. The sperm-specific features of meiosis revealed here illuminate how the underlying molecular machinery required for meiosis is differentially regulated in each sex.
Sperm and oocytes contribute equal but unique complements of DNA to each new life. Both types of cells arise from meiosis, a multi-step program during which chromosomes replicate, pair and recombine, then divide to generate haploid gametes. Simultaneously, each cell type also differentiates via distinct developmental programs. Spermatogenesis rapidly produces many small, motile sperm with highly protected chromatin, while oogenesis occurs at a slower rate to yield fewer large, immobile, nutrient-rich oocytes. We provide a detailed molecular analysis of key landmark events of spermatogenesis and identify spermatogenesis-specific features of meiosis in the model organism C. elegans. We find that, as in many meiotic programs, C. elegans spermatogenesis includes a chromosome aggregation or “karyosome” phase. This extended stage provides a period for chromosome and microtubule remodeling prior to the meiotic divisions. Our analysis identifies several gamete-specific features of the meiotic program that may contribute to the differential timing, pace, and mechanics of meiotic progression. Our findings provide a foundation for understanding how differentiation influences meiosis, which is an essential step in identifying universal features required for reproductive success in all organisms.