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The genetics of adaptation for eight microvirid bacteriophages.

Rokyta DR, Abdo Z, Wichman HA - J. Mol. Evol. (2009)

Bottom Line: Despite this, final fitnesses did not vary significantly among replicates.A positive correlation was found between the number of substitutions in an adaptive walk and the magnitude of fitness improvement, but no correlation was found between starting and ending fitness.These results provide an empirical framework for future adaptation theory.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, University of Idaho, Moscow, ID 83844-3051, USA.

ABSTRACT
Theories of adaptive molecular evolution have recently experienced significant expansion, and their predictions and assumptions have begun to be subjected to rigorous empirical testing. However, these theories focus largely on predicting the first event in adaptive evolution, the fixation of a single beneficial mutation. To address long-term adaptation it is necessary to include new assumptions, but empirical data are needed for guidance. To empirically characterize the general properties of adaptive walks, eight recently isolated relatives of the single-stranded DNA (ssDNA) bacteriophage phiX174 (family Microviridae) were adapted to identical selective conditions. Three of the eight genotypes were adapted in replicate, for a total of 11 adaptive walks. We measured fitness improvement and identified the genetic changes underlying the observed adaptation. Nearly all phages were evolvable; nine of the 11 lineages showed a significant increase in fitness. However, fitness plateaued quickly, and adaptation was achieved through only three substitutions on average. Parallel evolution was rampant, both across replicates of the same genotype as well as across different genotypes, yet adaptation of replicates never proceeded through the exact same set of mutations. Despite this, final fitnesses did not vary significantly among replicates. Final fitnesses did vary significantly across genotypes but not across phylogenetic groupings of genotypes. A positive correlation was found between the number of substitutions in an adaptive walk and the magnitude of fitness improvement, but no correlation was found between starting and ending fitness. These results provide an empirical framework for future adaptation theory.

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Fitness improvement for all 11 experimental lineages. The diagonal line corresponds to a failure to increase fitness. The magnitude of fitness improvement is indicated by vertical displacement above the line. Phylogenetic groups (see Fig. 1) are designated with different symbols. Both initial and final fitnesses have standard errors less than 0.55 and are measured in population doublings per hour
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Fig2: Fitness improvement for all 11 experimental lineages. The diagonal line corresponds to a failure to increase fitness. The magnitude of fitness improvement is indicated by vertical displacement above the line. Phylogenetic groups (see Fig. 1) are designated with different symbols. Both initial and final fitnesses have standard errors less than 0.55 and are measured in population doublings per hour

Mentions: The capacity of an organism to adapt in the presence of a selective pressure is generally referred to as evolvability (Wagner and Altenberg 1996; Kirschner and Gerhart 1998; McBride et al. 2008). Nine of the 11 experimental lineages responded to selection as evidenced by significant improvement in fitness. All lineages except for NC41a and WA11a, our only representatives of the φX174-like group (Fig. 1), had a significantly higher final fitness than initial fitness (t test, one-sided, unequal variance, P < 0.01 Bonferroni corrected; P > 0.10 for NC41a and WA11a). Figure 2 shows the initial and final fitnesses of the 11 lineages; Table 1 provides an overall summary of the adaptations. At least six of the eight genotypes were evolvable given our experimental conditions and the amount of time allowed for a response to selection. The largest fitness gain was achieved by lineage ID2a, which increased its fitness by 13.5 doublings per hour. This corresponds to more than a 500-fold increase in the total number of progeny produced per phage in 40 min, our standard growth period. This genotype, however, began with a much lower fitness than any other genotype and also achieved the lowest final fitness. Lineages NC41a and WA11a did not appear to increase in fitness; the fitness differences between the beginning and end points were −0.3 and 1.4 doublings per hour, respectively. NC41 had the highest initial fitness of all of the genotypes; WA11 had the third highest initial fitness (Table 1). This possibly contributed to their failure to achieve significant fitness improvement. Either these two phages were already at a local fitness optimum for our conditions or adaptive mutations of large to moderate effect are not accessible under these population dynamics. The average improvement in fitness over all 11 lineages was 5.8 doublings per hour, or a 15-fold increase in the number of progeny per phage per growth period.Fig. 2


The genetics of adaptation for eight microvirid bacteriophages.

Rokyta DR, Abdo Z, Wichman HA - J. Mol. Evol. (2009)

Fitness improvement for all 11 experimental lineages. The diagonal line corresponds to a failure to increase fitness. The magnitude of fitness improvement is indicated by vertical displacement above the line. Phylogenetic groups (see Fig. 1) are designated with different symbols. Both initial and final fitnesses have standard errors less than 0.55 and are measured in population doublings per hour
© Copyright Policy
Related In: Results  -  Collection

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Fig2: Fitness improvement for all 11 experimental lineages. The diagonal line corresponds to a failure to increase fitness. The magnitude of fitness improvement is indicated by vertical displacement above the line. Phylogenetic groups (see Fig. 1) are designated with different symbols. Both initial and final fitnesses have standard errors less than 0.55 and are measured in population doublings per hour
Mentions: The capacity of an organism to adapt in the presence of a selective pressure is generally referred to as evolvability (Wagner and Altenberg 1996; Kirschner and Gerhart 1998; McBride et al. 2008). Nine of the 11 experimental lineages responded to selection as evidenced by significant improvement in fitness. All lineages except for NC41a and WA11a, our only representatives of the φX174-like group (Fig. 1), had a significantly higher final fitness than initial fitness (t test, one-sided, unequal variance, P < 0.01 Bonferroni corrected; P > 0.10 for NC41a and WA11a). Figure 2 shows the initial and final fitnesses of the 11 lineages; Table 1 provides an overall summary of the adaptations. At least six of the eight genotypes were evolvable given our experimental conditions and the amount of time allowed for a response to selection. The largest fitness gain was achieved by lineage ID2a, which increased its fitness by 13.5 doublings per hour. This corresponds to more than a 500-fold increase in the total number of progeny produced per phage in 40 min, our standard growth period. This genotype, however, began with a much lower fitness than any other genotype and also achieved the lowest final fitness. Lineages NC41a and WA11a did not appear to increase in fitness; the fitness differences between the beginning and end points were −0.3 and 1.4 doublings per hour, respectively. NC41 had the highest initial fitness of all of the genotypes; WA11 had the third highest initial fitness (Table 1). This possibly contributed to their failure to achieve significant fitness improvement. Either these two phages were already at a local fitness optimum for our conditions or adaptive mutations of large to moderate effect are not accessible under these population dynamics. The average improvement in fitness over all 11 lineages was 5.8 doublings per hour, or a 15-fold increase in the number of progeny per phage per growth period.Fig. 2

Bottom Line: Despite this, final fitnesses did not vary significantly among replicates.A positive correlation was found between the number of substitutions in an adaptive walk and the magnitude of fitness improvement, but no correlation was found between starting and ending fitness.These results provide an empirical framework for future adaptation theory.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, University of Idaho, Moscow, ID 83844-3051, USA.

ABSTRACT
Theories of adaptive molecular evolution have recently experienced significant expansion, and their predictions and assumptions have begun to be subjected to rigorous empirical testing. However, these theories focus largely on predicting the first event in adaptive evolution, the fixation of a single beneficial mutation. To address long-term adaptation it is necessary to include new assumptions, but empirical data are needed for guidance. To empirically characterize the general properties of adaptive walks, eight recently isolated relatives of the single-stranded DNA (ssDNA) bacteriophage phiX174 (family Microviridae) were adapted to identical selective conditions. Three of the eight genotypes were adapted in replicate, for a total of 11 adaptive walks. We measured fitness improvement and identified the genetic changes underlying the observed adaptation. Nearly all phages were evolvable; nine of the 11 lineages showed a significant increase in fitness. However, fitness plateaued quickly, and adaptation was achieved through only three substitutions on average. Parallel evolution was rampant, both across replicates of the same genotype as well as across different genotypes, yet adaptation of replicates never proceeded through the exact same set of mutations. Despite this, final fitnesses did not vary significantly among replicates. Final fitnesses did vary significantly across genotypes but not across phylogenetic groupings of genotypes. A positive correlation was found between the number of substitutions in an adaptive walk and the magnitude of fitness improvement, but no correlation was found between starting and ending fitness. These results provide an empirical framework for future adaptation theory.

Show MeSH