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Fitness effects of advantageous mutations in evolving Escherichia coli populations - PubMed

  • ️Mon Jan 01 2001

Fitness effects of advantageous mutations in evolving Escherichia coli populations

M Imhof et al. Proc Natl Acad Sci U S A. 2001.

Abstract

The central role of beneficial mutations for adaptive processes in natural populations is well established. Thus, there has been a long-standing interest to study the nature of beneficial mutations. Their low frequency, however, has made this class of mutations almost inaccessible for systematic studies. In the absence of experimental data, the distribution of the fitness effects of beneficial mutations was assumed to resemble that of deleterious mutations. For an experimental proof of this assumption, we used a novel marker system to trace adaptive events in an evolving Escherichia coli culture and to determine the selective advantage of those beneficial mutations. Ten parallel cultures were propagated for about 1,000 generations by serial transfer, and 66 adaptive events were identified. From this data set, we estimate the rate of beneficial mutations to be 4 x 10(-9) per cell and generation. Consistent with an exponential distribution of the fitness effects, we observed a large fraction of advantageous mutations with a small effect and only few with large effect. The mean selection coefficient of advantageous mutations in our experiment was 0.02.

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Figures

Figure 1
Figure 1

Allele frequencies for one of the ten replicate populations. During the entire experiment, every 90th generation, a “snapshot” of the allele distribution in the evolving population was taken. The number in the upper right corner of each diagram indicates the number of generations; error bars show standard deviations of three independent measurements. Each column indicates the frequency of the corresponding allele in the bacterial culture at a given time. The shown frequencies are based on approximately 5 × 108 cells. Arrows indicate the alleles, which significantly increase in frequency. All significant increases are consecutively numbered.

Figure 2
Figure 2

Experimental reproduction of selective sweeps, which were identified by a statistically significant change in allele frequency. (a and b) The replication of a significant increase in allele frequency, which reaches a high frequency. (c and d) The replication of a significant increase in allele frequency, which does not reach a high frequency. For each replication experiment, five replicate cultures were inoculated from a frozen stock (representing generation 378 in the original culture for the high frequency event, 108 for the low frequency event respectively). Allele frequency distributions are shown after 18 generations (a and c) and 90 generations (b and d) of independent propagation of the replicate cultures. Replicas were analyzed and tested for significant allele frequency shifts. In all replicate cultures, significant change in allele frequency was observed for the allele carrying 29 repeats (a and b) and for the 11-repeat allele (c and d). Arrows indicate the alleles, that significantly increase in frequency.

Figure 3
Figure 3

Distribution of selection coefficients combined over 1,000 generations and 10 experimental cultures. Selection coefficients smaller than 0.01 were not included, because most of them could not be discriminated from experimental errors. It should be noted that all selection coefficients were determined without accounting for clonal interference.

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