Mutational divergence over years in local populations of the selfing nematode Caenorhabditis elegans

Laboratory mutation accumulation experiments allow the assessment of spontaneous mutation rates and patterns with minimal selection. Here, we aimed to follow the accumulation and fate of mutations in natural populations, in a spatial context. The nematode Caenorhabditis elegans is particularly suited for such endeavor, as it reproduces almost exclusively by selfing. We analyzed the evolution of clonal C. elegans genotypes along a 300-m-long stream bank in the Santeuil wood (France), based on short-read whole-genome sequencing of individuals collected between 2009 and 2022. We monitored along years the evolution of two of these quasi-clones, composed of individuals only differing by recent mutations. Recombination was scarce. A temporal signal was detected: strains from earlier years were found close to inner nodes of the tree, while recent ones were found on outer tips. This signal allowed us to estimate a substitution rate of 4 to 5 × 10-8 mutations per base pair per year, which can be used to calibrate divergence times among and within species. Mutation densities were higher on the X chromosome, on chromosome arms, and in non-exonic regions. We detected a high transition-to-transversion ratio, not observed in C. elegans laboratory mutation accumulation lines. Based on the spontaneous mutation rate per generation in laboratory lines of intergenic regions under minimal purifying selection, we estimated that C. elegans locally undergoes around 25 effective generations per year. Finally, using these recent mutations, we detected a spatiotemporal pattern within the field site, indicating limited dispersal at the scale of 100 m within 10 years.