Programmed DNA elimination was present in the last common ancestor of Caenorhabditis nematodes

In most organisms, all cells inherit the same genome, and many mechanisms exist to preserve genome integrity across cell divisions. However, some species undergo programmed DNA elimination (PDE), whereby specific genome regions are removed from somatic cell lineages early during development, leading to distinct germline and somatic genomes. Since its discovery in parasitic nematodes over a century ago, PDE has been observed in diverse eukaryotes, including ciliates, arthropods, and vertebrates. However, the function, mechanisms, and evolutionary origins of PDE remain poorly understood. Here, we report the unexpected discovery of PDE in three early-diverging Caenorhabditis species. Using long-read and chromatin conformation capture sequencing, we reconstructed germline and somatic genomes for all three species, and found that between 0.7 and 2.3% of the genome is eliminated during the 8- to 16-cell stage of embryogenesis, including the telomeres and regions within chromosomes. Elimination of regions within chromosomes results in fragmentation of the six germline chromosomes into 8-15 somatic chromosomes. The sites of elimination are precise, and we identified conserved motifs that likely recruit a nuclease to induce double-strand breaks. The newly formed somatic chromosome ends are healed by de novo telomere addition. A small number of genes are eliminated in each species, some of which have C. elegans orthologues with essential germline functions. A subset of elimination sites are orthologous across species, and some coincide with genome rearrangement sites. The phylogenetic distribution of PDE suggests that it was present in the last common Caenorhabditis ancestor and subsequently lost early during the evolution of many species, including C. elegans .