Mutational divergence 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 study 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 followed along years two distinct clones (isotypes), 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. Based on the spontaneous mutation rate per generation in laboratory lines, we estimated that C. elegans locally undergoes around 25 effective generations 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. Finally, using these recent mutations, we detected a spatio-temporal pattern within the field site, indicating limited dispersal at the scale of 100 meters within 10 years.