T2T genomes of Caenorhabditis nigoni and Caenorhabditis briggsae reveals extensive loss of satellite DNA associated with self-fertilization

Abstract

The two closely related Caenorhabditis nematode species, C. nigoni and C. briggsae, are commonly used to study the evolution of reproductive modes in animals, with the self-fertile C. briggsae and outcrossing C. nigoni sharing a common ancestor [~]3.5 million years ago. Earlier genomic analyses of these species revealed genome shrinkage associated with selfing and proposed that at least some gene loss can be adaptive. However, the incomplete C. nigoni reference genome limited most comparative analyses to genic regions. Here, we leveraged long-read sequencing to generate a telomere-to-telomere (T2T) assembly for the C. nigoni strain JU1422 and the C. briggsae strain AF16. This new 139Mb C. nigoni genome resolved 57 gaps and 149 unassigned scaffolds from the previous genome assembly. Comparison with the 107Mb T2T C. briggsae genome reveals that the major driver of genome content differences are deletions to satellite DNA arrays, reflecting a loss of 9.6Mb. Interestingly, many of the differences are on the C. nigoni X chromosome, which is >13Mb larger than in the previous assembly. The transition to selfing was thus accompanied by a 37% reduction in the size of the sex chromosome compared to 16-21% shrinkage of the autosomes. We also document a surprising degree of plasticity in the ribosomal DNA, with the X chromosome harboring a second 45S rDNA array that is absent in C. briggsae. Our analysis reveals that obligatory outcrossing may play a major role in the maintenance of satellite DNA arrays.