Piano, Fabio, Corcoran, David, Gunsalus, Kristin, Kovtun, Mikhail, Gutwein, Michelle, Zegar, Charles, Fradin, Helene, Baugh, Ryan, Lucas, Jessica, Fitch, David, Kiontke, Karin
[
International Worm Meeting,
2017]
Long-lived clades of animals that reproduce exclusively asexually are rare, presumably because lack of variation in such species results in high extinction rates. Longevity of asexual clades appears to be correlated with the maintenance of heterozygosity across generations. To understand how successful asexual lineages evolve while maintaining heterozygosity, we investigated the reproductive biology and genome sequence of the nematode Diploscapter coronatus. D. coronatus is a species that belongs to the Protorhabditis group, the sister group to Caenorhabditis. We confirmed the existence of a long-lived (approx. 18 million years) asexual clade within Protorhabditis and resolved its phylogeny. We found that all asexual species in the clade have an unusual karyotype: a single pair of chromosomes. This karyotype evolved once from an ancestor with six chromosome pairs. This drastic drop in the number of chromosomes coincides with the transition from sexual to asexual reproduction. We determined the D. coronatus genome structure and sequence, and find evidence in the genome assembly that the single chromosome resulted from the fusion of ancestral chromosomes. This fusion is associated with extensive rearrangement among neighboring regions, which we used to infer a partial spatial order in which ancestral chromosomes fused. The genome can be organized into two divergent homologous haplotypes, confirming that heterozygosity is maintained in this species despite the asexual reproduction. Interestingly, two adjacent fused regions, corresponding to ancestral chromosomal domains I and X, show lower levels of heterozygosity than the other domains. These data are consistent with a scenario in which an initial X-I fusion became a neo-X chromosome in a sexual ancestor. This neo-X would have had a reduced effective population size and thus reduced heterozygosity and increased linkage disequilibrium relative to the autosomes. Consistent with chromosomal fusions, we find no evidence of typical nematode telomeres in the D. coronatus genome. Parthenogenesis likely evolved after chromosomal fusion. Cytological observations indicate that D. coronatus reproduces with a modified meiosis that skips Meiosis I, synapsis and recombination and results in a diploid embryo without fertilization. Consistent with this model, certain key conserved genes with roles in homologous pairing and recombination were not found in the D. coronatus genome. Also, oogenesis without Meiosis I is one way in which parthenogenetic organisms can maintain heterozygosity. As a prelude to functional studies, we also show that D. coronatus is amenable to experimental manipulation by RNAi.