Spontaneous mutational and standing genetic (co)variation at dinucleotide microsatellites in Caenorhabditis briggsae and Caenorhabditis elegans

Abstract

Understanding the evolutionary processes responsible for shaping genetic variation within and between species requires separating the effects of mutation and selection. Differences between the patterns of genetic variation observed in nature and when mutations are allowed to accumulate in the relative absence of selection can reveal biases imposed by selection. We characterize the genetic variation at dinucleotide microsatellite repeats in four sets of 250-generation mutation accumulation (MA) lines, two in the species Caenorhabditis briggsae and two in Caenorhabditis elegans, and compare the mutational variation with the standing variation in those species. We also compare the mutational properties of microsatellites with the cumulative effects of mutations on fitness in the same lines. Integrated over the whole genome, we infer that the mutation rate of C. briggsae is about twice that of C. elegans, consistent with the cumulative mutational effects on fitness. The mutational spectrum (ratio of insertions to deletions) differs between repeat types and, in some cases, between species. The per-locus mutation rate is significantly positively correlated with the standing genetic variation at the same locus in both species, providing justification for the common practice of using the standing genetic variance as a surrogate for the mutation rate.

FIG. 1.—

Relationship between observed mutation rate (μ_OBS; dependent variable) and number of perfect repeats (independent variable) for each repeat type in the two strains Caenorhabditis briggsae and Caenorhabditis elegans. Panels A–C are of AC, AG, and AT repeats in the HK104 (diamonds) and PB800 (squares) strains of C. briggsae. Solid and dashed lines are the best-fit linear regression of μ_OBS on repeat number in HK104 and PB800, respectively. Panels D–F are of AC, AG, and AT repeats in the N2 (diamonds) and PB306 (squares) strains of C. elegans. Solid and dashed lines are the regression of μ_OBS on repeat number in N2 and PB306, respectively.

FIG. 2.—

Genomewide distribution of dinucleotide STR loci in (A) the Caenorhabditis elegans and (B) the Caenorhabditis briggsae genomes. Only perfect repeats are reported. The Y-axis is the frequency in the genome. The X-axis is divided into bins of five repeats, with all loci greater than 60 repeats pooled.