Male meiotic spindle features that efficiently segregate paired and lagging chromosomes

Chromosome segregation during male meiosis is tailored to rapidly generate multitudes of sperm. Little, however, is known about the mechanisms that efficiently segregate chromosomes to produce sperm. Using live imaging in Caenorhabditis elegans , we find that spermatocytes exhibit simultaneous pole-to-chromosome shortening (anaphase A) and pole-to-pole elongation (anaphase B). Electron tomography unexpectedly revealed that spermatocyte anaphase A does not stem from kinetochore microtubule shortening. Instead, movement is driven by changes in distance between chromosomes, microtubules, and centrosomes upon tension release at anaphase onset. We also find that the lagging X chromosome, a distinctive feature of anaphase I in C. elegans males, is due to lack of chromosome pairing. The unpaired chromosome remains tethered to centrosomes by continuously lengthening kinetochore microtubules which are under tension, suggesting a ‘tug of war’ that can reliably resolve chromosome lagging. Overall, we define features that partition both paired and lagging chromosomes for optimal sperm production.