Genome Architecture and Evolution of a Unichromosomal Asexual Nematode

Asexual reproduction in animals, though rare, is the main or exclusive mode of reproduction in some long-lived lineages. The longevity of asexual clades may be correlated with the maintenance of heterozygosity by mechanisms that rearrange genomes and reduce recombination. Asexual species thus provide an opportunity to gain insight into the relationship between molecular changes, genome architecture, and cellular processes. Here we report the genome sequence of the parthenogenetic nematode Diploscapter pachys with only one chromosome pair. We show that this unichromosomal architecture is shared by a long-lived clade of asexual nematodes closely related to the genetic model organism Caenorhabditis elegans. Analysis of the genome assembly reveals that the unitary chromosome arose through fusion of six ancestral chromosomes, with extensive rearrangement among neighboring regions. Typical nematode telomeres and telomeric protection-encoding genes are lacking. Most regions show significant heterozygosity; homozygosity is largely concentrated to one region and attributed to gene conversion. Cell-biological and molecular evidence is consistent with the absence of key features of meiosis I, including synapsis and recombination. We propose that D. pachys preserves heterozygosity and produces diploid embryos without fertilization through a truncated meiosis. As a prelude to functional studies, we demonstrate that D. pachys is amenable to experimental manipulation by RNA interference. [Display omitted] •Asexuality and a single chromosome evolved around the same time in Diploscapter•The single chromosome resulted from fusions of six ancestral chromosomes•Meiosis is truncated and many meiosis and telomere maintenance genes are missing•These features have most likely favored the evolution of significant heterozygosity By genome sequencing, Fradin et al. discover that the single chromosome in an asexual group of nematodes resulted from a fusion of six ancestral chromosomal domains. Due to the lack of recombination between alleles at most loci, high heterozygosity has evolved, providing one explanation for the unexpected longevity of this asexual lineage.