Degradation of the Repetitive Genomic Landscape in a Close Relative of Caenorhabditis elegans.

The abundance, diversity, and genomic distribution of repetitive elements is highly variable among species. These patterns are thought to be driven in part by reproductive mode and the interaction of selection and recombination, and recombination rates typically vary by chromosomal position. In the nematode Caenorhabditis elegans, repetitive elements are enriched at chromosome arms and depleted on centers, and this mirrors the chromosomal distributions of other genomic features such as recombination rate. How conserved is this genomic landscape of repeats, and what evolutionary forces maintain it? To address this, we compared the genomic organization of repetitive elements across five Caenorhabditis species with chromosome-level assemblies. As previously reported, repeat content is enriched on chromosome arms in most Caenorhabditis species, and no obvious patterns of repeat content associated with reproductive mode were observed. However, the fig-associated C. inopinata has experienced repetitive element expansion and reveals no association of global repeat density with chromosome position. Patterns of repeat superfamily specific distributions reveal this global pattern is driven largely by a few repeat superfamilies that in C. inopinata have expanded in number and have weak associations with chromosome position. Additionally, 15% of predicted protein-coding genes in C. inopinata align to transposon-related proteins. When these are excluded, C. inopinata has no enrichment of genes in chromosome centers, in contrast to its close relatives who all have such clusters. Forward evolutionary simulations reveal that chromosomal heterogeneity in recombination rate alone can generate structured repetitive genomic landscapes when insertions are weakly deleterious, whereas chromosomal heterogeneity in the fitness effects of transposon insertion can promote such landscapes across a variety of evolutionary scenarios. Thus, patterns of gene density along chromosomes likely contribute to global repetitive landscapes in this group, although other historical or genomic factors are needed to explain the idiosyncrasy of genomic organization of various transposable element taxa within C. inopinata. Taken together, these results highlight the power of comparative genomics and evolutionary simulations in testing hypotheses regarding the causes of genome organization.