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Despite the fundamental importance of mutation to the evolutionary process, we have little knowledge of the direct consequences of specific spontaneous mutations to the fitness of the organism. Combining results of whole-genome sequencing with repeated field assays of survival and reproduction, we quantify the combined effects on fitness of spontaneous mutations identified in Arabidopsis thaliana. We demonstrate that the effects are beneficial, deleterious, or neutral depending on the environmental context. Some lines, bearing mutations disrupting known loci, differ strongly in fitness from the founder or premutation genotype. Those effects vary across environments, for example, a line with a major deletion spanning a transcription factor gene expressed lower fitness than the founder under most conditions but exceeded the founder's fitness in one environment. The large contribution of genotype by environment interaction (G × E) to mutation effects on fitness implies spatial and/or temporal variation in selection on new mutations and could contribute to the maintenance of standing genetic variation.

Spontaneous deleterious mutation has been measured in a handful of organisms, always under laboratory conditions and usually employing inbred species or genotypes. We report the results of a mutation accumulation experiment with an outbred annual plant, Raphanus raphanistrum, with lifetime fitness measured in both the field and the greenhouse. This is the first study to report the effects of spontaneous mutation measured under field conditions. Two large replicate populations (N(e) approximately 600) were maintained with random mating in the greenhouse under relaxed selection for nine generations before the field assay was performed and ten generations before the greenhouse assay. Each generation, every individual was mated twice, once as a pollen donor and once as a pollen recipient, and a single seed from each plant was chosen randomly to create the next generation. The ancestral population was maintained as seeds at 4 degrees C. Declines in lifetime fitness were observed in both the field (1.7% per generation; P= 0.27) and the greenhouse (0.6% per generation; P= 0.07). Significant increases in additive genetic variance for fitness were found for stems per day, flowers per stem, fruits per flower and seeds per fruit in the field as well as for fruits per flower in the greenhouse. Lack of significance of the fitness decline may be due to the short period of mutation accumulation, the use of outbred populations, or both. The percent declines in fitness are at the high end of the range observed in other mutation accumulation experiments and give some support to the idea that mutational effects may be magnified under harsher field conditions. Thus, measurement of mutational parameters under laboratory conditions may underestimate the effects of mutations in natural populations.

Derived characters that have not changed during the diversification of a clade provide traits that are diagnostic at higher taxonomic levels. The tetradynamous stamen condition (four long and two short stamens) of the Brassicaceae is an example of a diagnostic trait that has not changed during the diversification of this large flowering plant family. We investigated one hypothesis that might explain the long-term stasis of this trait—that tetradynamous stamens have persisted because of an absence of genetic variation underlying the trait. Through a sib-analysis with Raphanus raphanistrum and an artificial selection experiment with Brassica rapa, we demonstrate that significant genetic variation is present for the tetradynamous condition in both species and that the trait is therefore not constrained from evolutionary change by a lack of heritable genetic variation.

It has often been suggested that selection on floral traits in hermaphroditic plants should occur primarily through differences in male fitness. However, measurements of selection on floral traits through differences in lifetime male fitness have been lacking. We measured selection on a variety of wild radish floral traits using lifetime male fitness measures derived from genetic paternity analysis. These male fitness estimates were then combined with estimates of lifetime female fitness of the same plants to produce measurements of selection based on lifetime total fitness. Contrary to the prediction above, there was no strong evidence for selection on floral morphology through male fitness differences in any of the three years of the study, but there was strong selection for increased flower size through female fitness differences in one year. The main determinant of both male and female fitness in all years was flower number; this lead to moderately positive correlations between male and female fitness in all three years.