Non-Mendelian assortment of homologous autosomes of different sizes in males is the ancestral state in the Caenorhabditis lineage

Organismal genome sizes vary by six orders of magnitude and appear positively correlated with organismal size and complexity. Neutral models have been proposed to explain the broad patterns of genome size variation based on organism population sizes. In the Caenorhabditis genus, hermaphrodite genomes are smaller than those of gonochoristic species. One possible driving force for this genome size difference could be non-random chromosome segregation. In Caenorhabditis elegans, chromosome assortment is non-independent and violates Mendel’s second law. In males, the shorter homologue of a heterozygous autosome pair preferentially co-segregates with the X chromosome while the longer one preferentially co-segregates with the nullo-X (O) chromosome in a process we call “skew”. Since hermaphrodites preferentially receive the shorter chromosomes and can start populations independently, their genome size would be predicted to decrease over evolutionary time. If skew is an important driver for genome size reduction in hermaphroditic Caenorhabditis species, then it should be present in all congeneric species. In this study, we tested this hypothesis and found that skew is present in all eight examined species. Our results suggest that skew is likely the ancestral state in this genus. More speculatively, skew may drive genome size patterns in hermaphroditic species in other nematodes.