The genome architecture of unichromosomal parthenogenetic nematode Diploscapter sp. 1---a close relative of model organism Caenorhabditis elegans

Asexually reproducing species, though less prevalent than sexually reproducing ones, exist across the whole eukaryotic domain; they have both ecological and medical relevance because many parasites of plants and animals reproduce asexually. These species are short-lived compared to their sexually reproducing counterparts. However, there is no unifying theory to explain this relative success of sex, perhaps due to the diversity of asexuals. With the advent of the genomic era, analyses of the genome architecture of a limited number of asexually reproducing species found that they can be subject to multiple chromosomal rearrangements. Therefore, understanding their genomic architecture might be key to understand how asexuals evolve from sexual ancestors, how they resist some environmental changes but go extinct prematurely.;Well-studied asexual lineages typically lack proximity to a well-studied sexual relative that allows for comparative studies. A successful asexual lineage evolved within the Protorhabditis group of nematodes and represents the closest transition to asexual reproduction relative to the sexually reproducing model organism Caenorhabditis elegans. One species from this lineage has been described with a single pair of homologous chromosomes, a very rare occurrence in eukaryotes.;In this work, I report the genome sequence of the unichromosomal asexually reproducing species Diploscapter sp. 1 from the Protorhabditis group and use it to study the evolution of a successful asexual lineage and its genome architecture. I show that species that reproduce asexually in the group share the same unichromosomal karyotype, while sexually reproducing ones have six or seven chromosomes like C. elegans. I demonstrate that the single chromosome in Diploscapter sp. 1 results from a chromosomal fusion and infer a partial spatial order in which ancestral chromosomes fused. Analyzing repeat motifs and gene content, I find a candidate mechanism to explain chromosomal fusion as telomere structure is shown to be highly divergent in Diploscapter sp. 1. Homologous pairing of chromosomes and recombination machinery also diverged, consistent with a model of asexual reproduction where embryos are generated through a unique division akin to mitosis but retaining some meiotic features. This model also explains the high heterozygosity observed in the genome as it maintains both diploidy and heterozygosity from one generation to the next.;Together, these results are consistent with the idea that asexually reproducing species can display very distinctive genome architectures outside the scope of conventional meiosis. This study exposes connections between molecular changes and specific perturbations in meiosis, stressing the omnipresence in the life cycle of every eukaryote of meiosis even when disrupted.