The unequal partitioning of molecules and organelles during cell division results in daughter cells with different fates. An extreme example is female meiosis, in which consecutive asymmetric cell divisions give rise to one large oocyte and two small polar bodies with DNA and minimal cytoplasm. Here we test the hypothesis that during an asymmetric cell division during spermatogenesis of the nematode Auanema rhodensis, the late segregating X chromatids orient the asymmetric partitioning of cytoplasmic components. In previous studies, the secondary spermatocytes of wild type XO males were found to divide asymmetrically to generate functional spermatids that inherit components necessary for sperm viability and DNA-containing residual bodies that inherit components to be discarded. Here we extend that analysis to two novel contexts. First, the isolation and analysis of a strain of mutant XX pseudomales revealed that such animals have highly variable patterns of X chromatid segregation. The pattern of late segregating X chromatids nevertheless predicted the orientation of organelle partitioning. Second, while wild type XX hermaphrodites were known to produce both 1X and 2X sperm, here we show that spermatocytes within specific spermatogonial clusters exhibit two different patterns of X chromatid segregation that correlate with distinct patterns of organelle partitioning. Together this analysis suggests that A. rhodensis has co-opted lagging X chromosomes during anaphase II as a mechanism for determining the orientation of organelle partitioning.

The unequal partition of molecules and organelles during cell division results in daughter cells with different fates. Asymmetric cell divisions have been best characterised in systems in which extrinsic signals polarise the mother cell during cell division. However, the mechanisms of asymmetric cell division mediated by intrinsic signals, and the nature of these signals, are mostly unknown. Here we report an asymmetric cell division in the nematode Auanema rhodensis that may be cued by the X chromosome. In the wildtype XO male, the spermatocyte divides asymmetrically to generate X-bearing spermatids that inherit components necessary for sperm viability, and nullo-spermatids that inherits components to be discarded. We found that in XX mutant pseudomales, sperm components co-segregate with the X chromosome, supporting the hypothesis that the X chromosome is employed as a polarising signal for partitioning essential cytoplasmic components for sperm function.

Auanema freiburgenseis a trioecious nematode with co-existing males, females, and selfing hermaphrodites. Crosses of XO males with XX females result in a low percentage of XO sons (<20%) due to the unusual male spermatogenesis that yields viable 1X sperm and non-viable nullo-X spermatids. However, intercrossing two strains ofA. freiburgenseresults in lines in which males produce viable nullo-X sperm, resulting in a high percentage (∼30-50%) of sons after crosses with females. We generated a genome assembly forA. freiburgenseand genotyped the intercrossed lines to uncover the genetic basis for this transgressive phenotype. We found a QTL on the X chromosome associated with the unusual spermatogenesis inA. freiburgense, providing a mechanistic basis for asymmetric partitioning of organelles during the male meiotic division.