A QTL influences sex ratios by controlling asymmetric organelle positioning during male spermatogenesis in Auanema freiburgense

Auanema freiburgense is 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 due to the elimination of the nullo-X spermatids by the fathers. This process yields most viable sperm containing an X chromosome, leading to a higher transmission probability of the X chromosome compared to expected transmission via random segregation. The mechanism underlying this process involves the asymmetric distribution of essential cellular organelles during sperm formation, which likely depends on the X chromosome. Specifically, sperm components segregate with the X chromosome daughter cell, while other components are discarded in the nullo-X daughter cell. Here we found that intercrossing two strains of A. freiburgense results in lines in which males produce viable nullo-X sperm. Thus, crosses of those hybrid males with females result in a high percentage of sons. To uncover the genetic basis of nullo-spermatid elimination and X-chromosome drive, we generated a genome assembly for A. freiburgense and genotyped the intercrossed lines. We identified a QTL encompassing several genes on the X chromosome that are associated with its non-Mendelian inheritance observed in A. freiburgense. This finding provides valuable clues to the underlying factors involved in asymmetric organelle partitioning during male meiotic division and thus non-Mendelian transmission of the X chromosome and sex ratios.