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The hermaphroditic nematode Caenorhabditis elegans has been one of the primary model systems in biology since the 1970s, but only within the last two decades has this nematode also become a useful model for experimental evolution. Here, we outline the goals and major foci of experimental evolution with C. elegans and related species, such as C . briggsae and C. remanei , by discussing the principles of experimental design, and highlighting the strengths and limitations of Caenorhabditis as model systems. We then review three exemplars of Caenorhabditis experimental evolution studies, underlining representative evolution experiments that have addressed the: (1) maintenance of genetic variation; (2) role of natural selection during transitions from outcrossing to selfing, as well as the maintenance of mixed breeding modes during evolution; and (3) evolution of phenotypic plasticity and its role in adaptation to variable environments, including host-pathogen coevolution. We conclude by suggesting some future directions for which experimental evolution with Caenorhabditis would be particularly informative., (Copyright © 2017 Teotónio et al.)

Mutation rate often increases with environmental temperature, but establishing causality is complicated. Asymmetry between physiological stress and deviation from the optimal temperature means that temperature and stress are often confounded. We allowed mutations to accumulate in two species of Caenorhabditis for approximately 100 generations at 18°C and for approximately 165 generations at 26°C; 26°C is stressful for Caenorhabditis elegans but not for Caenorhabditis briggsae. We report mutation rates at a set of microsatellite loci and estimates of the per-generation decay of fitness (ΔM(w)), the genomic mutation rate for fitness (U) and the average effect of a new mutation (E[a]), assayed at both temperatures. In C. elegans, the microsatellite mutation rate is significantly greater at 26°C than at 18°C whereas in C. briggsae there is only a slight, non-significant increase in mutation rate at 26°C, consistent with stress-dependent mutation in C. elegans. The fitness data from both species qualitatively reinforce the microsatellite results. The fitness results of C. elegans are potentially complicated by selection but also suggest temperature-dependent mutation; the difference between the two species suggests that physiological stress plays a significant role in the mutational process.

Evolutionary theory predicts that the strength of natural selection to reduce the mutation rate should be stronger in self-fertilizing than in outcrossing taxa. However, the relative efficacy of selection on mutation rate relative to the many other factors influencing the evolution of any species is poorly understood. To address this question, we allowed mutations to accumulate for ∼100 generations in several sets of "mutation accumulation" (MA) lines in three species of gonochoristic (dieocious) Caenorhabditis (C. remanei, C. brenneri, C. sp. 5) as well as in a dioecious strain of the historically self-fertile hermaprohodite C. elegans. In every case, the rate of mutational decay is substantially greater in the gonochoristic taxa than in C. elegans (∼4× greater on average). Residual heterozygosity in the ancestral controls of these MA lines introduces some complications in interpreting the results, but circumstantial evidence suggests the results are not primarily due to inbreeding depression resulting from residual segregating variation. The results suggest that natural selection operates to optimize the mutation rate in Caenorhabditis and that the strength (or efficiency) of selection differs consistently on the basis of mating system, as predicted by theory. However, context-dependent environmental and/or synergistic epistasis could also explain the results., (© 2010 The Author(s). Evolution© 2010 The Society for the Study of Evolution.)

Genetic and developmental architecture may bias the mutationally available phenotypic spectrum. Although such asymmetries in the introduction of variation may influence possible evolutionary trajectories, we lack quantitative characterization of biases in mutationally inducible phenotypic variation, their genotype-dependence, and their underlying molecular and developmental causes. Here we quantify the mutationally accessible phenotypic spectrum of the vulval developmental system using mutation accumulation (MA) lines derived from four wild isolates of the nematodes Caenorhabditis elegans and C. briggsae. The results confirm that on average, spontaneous mutations degrade developmental precision, with MA lines showing a low, yet consistently increased, proportion of developmental defects and variants. This result indicates strong purifying selection acting to maintain an invariant vulval phenotype. Both developmental system and genotype significantly bias the spectrum of mutationally inducible phenotypic variants. First, irrespective of genotype, there is a developmental bias, such that certain phenotypic variants are commonly induced by MA, while others are very rarely or never induced. Second, we found that both the degree and spectrum of mutationally accessible phenotypic variation are genotype-dependent. Overall, C. briggsae MA lines exhibited a two-fold higher decline in precision than the C. elegans MA lines. Moreover, the propensity to generate specific developmental variants depended on the genetic background. We show that such genotype-specific developmental biases are likely due to cryptic quantitative variation in activities of underlying molecular cascades. This analysis allowed us to identify the mutationally most sensitive elements of the vulval developmental system, which may indicate axes of potential evolutionary variation. Consistent with this scenario, we found that evolutionary trends in the vulval system concern the phenotypic characters that are most easily affected by mutation. This study provides an empirical assessment of developmental bias and the evolution of mutationally accessible phenotypes and supports the notion that such bias may influence the directions of evolutionary change., Competing Interests: The authors have declared that no competing interests exist.

The evolutionary mechanisms maintaining genetic variation in life span, particularly post-reproductive life span, are poorly understood. We characterized the effects of spontaneous mutations on life span in the rhabditid nematodes Caenorhabditis elegans and C. briggsae and standing genetic variance for life span and correlation of life span with fitness in C. briggsae. Mutations decreased mean life span, a signature of directional selection. Mutational correlations between life span and fitness were consistently positive. The average selection coefficient against new mutations in C. briggsae was approximately 2% when homozygous. The pattern of phylogeographic variation in life span is inconsistent with global mutation-selection balance (MSB), but MSB appears to hold at the local level. Standing genetic correlations in C. briggsae reflect mutational correlations at a local scale but not at a broad phylogeographic level. At the local scale, results are broadly consistent with predictions of the "mutation accumulation" hypothesis for the evolution of aging.

The genetic variation present in a species depends on the interplay between mutation, population size, and natural selection. At mutation-(purifying) selection balance (MSB) in a large population, the standing genetic variance for a trait (VG) is predicted to be proportional to the mutational variance for the trait (VM); VM is proportional to the mutation rate for the trait. The ratio VM/VG predicts the average strength of selection (S) against a new mutation. Here we compare VM and VG for lifetime reproductive success (approximately fitness) and body volume in two species of self-fertilizing rhabditid nematodes, Caenorhabditis briggsae and C. elegans, which the evidence suggests have different mutation rates. Averaged over traits, species, and populations within species, the relationship between VG and VM is quite stable, consistent with the hypothesis that differences among groups in standing variance can be explained by differences in mutational input. The average (homozygous) selection coefficient inferred from VM/VG is a few percent, smaller than typical direct estimates from mutation accumulation (MA) experiments. With one exception, the variance present in a worldwide sample of these species is similar to the variance present within a sample from a single locale. These results are consistent with specieswide MSB and uniform purifying selection, but genetic draft (hitchhiking) is a plausible alternative possibility.

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.

It is often assumed that the mutation rate is an evolutionarily optimized property of a taxon. The relevant mutation rate is for mutations that affect fitness, U, but the strength of selection on the mutation rate depends on the average effect of a mutation. Determination of U is complicated by the possibility that mutational effects depend on the particular environmental context in which the organism exists. It has been suggested that the effects of deleterious mutations are typically magnified in stressful environments, but most studies confound genotype with environment, so it is unclear to what extent environmental specificity of mutations is specific to a particular starting genotype. We report a study designed to separate effects of species, genotype, and environment on the degradation of fitness resulting from new mutations. Mutations accumulated for >200 generations at 20 degrees in two strains of two species of nematodes that differ in thermal sensitivity. Caenorhabditis briggsae and C. elegans have similar demography at 20 degrees, but C. elegans suffers markedly reduced fitness at 25 degrees. We find little evidence that mutational properties differ depending on environmental conditions and mutational correlations between environments are close to those expected if effects were identical in both environments.