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.

In contrast to their dioecious relatives, members of the parthenogenetic Diploscapter nematode genus harbour their entire genome within a single pair of highly heterozygous chromosomes. To examine how this unusual karyotype relates to the evolution of parthenogenesis, we generated chromosome-level assemblies for two species in this clade: Diploscapter pachys and Diploscapter coronatus. Sequence comparisons revealed that the two genomes are colinear across their entirety, and that multiple ancestral chromosome fusions and extensive genomic rearrangements preceded the divergence of these two species. The presence of shortened telomeres and extended subtelomeric repeats suggests that the fusions arose from defects in telomere function in the lineage. Our analysis also identified an introgression event after divergence of the two species, suggesting that their parthenogenetic lifestyle may have been punctuated by rare sexual reproduction. These findings shed new light on how telomere loss, chromatin architecture, and reproductive strategies interconnect in shaping chromosome evolution.

How do sex chromosomes evolve in the transition to asexuality? So far, species that depart from canonical sexual reproduction - for example, parthenogens with rare sex, or species where the paternal genome is set aside - have been found to carry either no sex chromosomes, or sex chromosomes but no male-specific sex chromosome (i. e., no Y). Here we reveal that, in Mesorhabditis nematodes, a new Y chromosome emerged once, from sexual ancestors, in species that have transitioned into an unconventional mode of reproduction called autopseudogamy. In this reproductive system, females produce clonal females plus rare ([~]10%) males that are needed for fertilisation, but that do not contribute to the female genome. Analysing the Y chromosomes of two autopseudogamous species, we found high levels of degeneration, most likely due to loss of recombination, and two additional conserved features: i) they accumulated male-beneficial genes, and ii) they display a strong fertilisation drive, in that mainly Y-bearing sperm fertilise female oocytes. Both features are likely evolutionarily favourable in the context of autopseudogamy. Our results suggest that male-specific chromosomes can still be maintained in systems with rare, and possibly genetically useless, males.

Host-parasite interactions exert strong selection pressures on the genomes of both host and parasite. These interactions can lead to negative frequency-dependent selection, a form of balancing selection that is hypothesised to explain the high levels of polymorphism seen in many host immune and parasite antigen loci. Here, we sequence the genomes of several individuals of Heligmosomoides bakeri, a model parasite of house mice, and Heligmosomoides polygyrus, a closely related parasite of wood mice. Although H. bakeri is commonly referred to as H. polygyrus in the literature, their genomes show levels of divergence that are consistent with at least a million years of independent evolution. The genomes of both species contain hyper-divergent haplotypes that are enriched for proteins that interact with the host immune response. Many of these haplotypes originated prior to the divergence between H. bakeri and H. polygyrus, suggesting that they have been maintained by long-term balancing selection. Together, our results suggest that the selection pressures exerted by the host immune response have played a key role in shaping patterns of genetic diversity in the genomes of parasitic nematodes.

Heteromorphic sex chromosomes are usually thought to have originated from a pair of autosomes that acquired a sex-determining locus and subsequently stopped recombining, leading to degeneration of the sex-limited chromosome. The majority of nematode species lack heteromorphic sex chromosomes and determine sex using an X-chromosome counting mechanism, with males being hemizygous for one or more X chromosomes (XX/X0). Some filarial nematode species, including important parasites of humans, have heteromorphic XX/XY karyotypes. It has been assumed that sex is determined by a Y-linked locus in these species. However, karyotypic analyses suggested that filarial Y chromosomes are derived from the unfused homologue of an autosome involved in an X-autosome fusion event. Here, we generated a chromosome-level reference genome for Litomosoides sigmodontis, a filarial nematode with the ancestral filarial karyotype and sex determination mechanism (XX/X0). By mapping the assembled chromosomes to the rhabditid nematode ancestral linkage (or Nigon) elements, we infer that the ancestral filarial X chromosome was the product of a fusion between NigonX (the ancestrally X-linked element) and NigonD (ancestrally autosomal). In the two filarial lineages with XY systems, there have been two independent X-autosome chromosome fusion events involving different autosomal Nigon elements. In both lineages, the region shared by the neo-X and neo-Y chromosomes is within the ancestrally autosomal portion of the X, confirming that the filarial Y chromosomes are derived from the unfused homologue of the autosome. Sex determination in XY filarial nematodes therefore likely continues to operate via the ancestral X-chromosome counting mechanism, rather than via a Y-linked sex-determining locus.