Genome Architecture and Evolution of a Unichromosomal Asexual Nematode

Abstract

SUMMARY 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 are 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 fertilizationthrough a truncated meiosis. As a prelude to functional studies, we demonstrate that D. pachys is amenable to experimental manipulation by RNA interference.

Clonal genome evolution and rapid invasive spread of the marbled crayfish

“…The transcriptome consists of 22,338 transcripts (Fig. 2c), which corresponds closely to the numbers of predicted genes (21,772) and messenger RNAs (22,205) in the genome assembly. Comparisons with other publicly available transcriptomes revealed homologues for the majority (81%) of predicted proteins, while 19% (n = 4,306) of the predicted proteins were classified as unique (Fig.…”

“…Their analysis revealed several interesting features that are likely to reflect important strategies for the evolutionary robustness of these parthenogenetic animals, including the presence of allelic regions on the same chromosome in A. vaga 23 and substantial heterozygosity, combined with the loss of key meiosis genes in Diploscapter pachys and Diploscapter coronatus 21,22 . However, these features were identified in genomes that have been shaped by asexual reproduction for millions of years.…”

“…Available genome sequences of parthenogenetic animals are currently limited to certain nematodes [19][20][21][22] and the bdelloid rotifer Adineta vaga 23 . Their analysis revealed several interesting features that are likely to reflect important strategies for the evolutionary robustness of these parthenogenetic animals, including the presence of allelic regions on the same chromosome in A. vaga 23 and substantial heterozygosity, combined with the loss of key meiosis genes in Diploscapter pachys and Diploscapter coronatus 21,22 .…”

Genomic features of parthenogenetic animals

“…pulex, they were estimated to amount to approximately 10 −6 locus −1 generation −1 [27,28,70], in the amazon molly P. formosa to 10 − 8 [17]. Up to 11% of the genome of the nematode D. pachys [32] is suggested to be homozygous as a consequence of gene conversion, and studies have also argued for an important role of gene conversion for genome evolution in root-knot nematodes [37] and rotifers [18,19], although no quantitative estimates are available for these groups.…”

“…The majority of meiosis genes was recovered in bdelloid rotifers [18,19], and furthermore nearly all genes were also absent in the sexual species, indicating that meiosis gene loss is not associated with the evolution of asexuality [98]. Diploscapter nematodes also lack certain meiosis genes, but it is unknown whether these genes are also missing in sexual relatives [31,32]. As much as the idea is appealing, there does not seem to be any support for the predicted loss of meiotic genes in mitotic asexuals.…”