2010
Cooper T F; Lenski R E
Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations Journal Article
BMC Evolutionary Biology, 10 (1), pp. 11, 2010, ISSN: 1471-2148.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Cooper2010,
title = {Experimental evolution with \textit{E. coli} in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations},
author = {Tim F. Cooper and Richard E. Lenski},
url = {http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-11},
doi = {10.1186/1471-2148-10-11},
issn = {1471-2148},
year = {2010},
date = {2010-01-01},
urldate = {2010-01-01},
journal = {BMC Evolutionary Biology},
volume = {10},
number = {1},
pages = {11},
abstract = {Background
Environmental conditions affect the topology of the adaptive landscape and thus the trajectories followed by evolving populations. For example, a heterogeneous environment might lead to a more rugged adaptive landscape, making it more likely that replicate populations would evolve toward distinct adaptive peaks, relative to a uniform environment. To date, the influence of environmental variability on evolutionary dynamics has received relatively little experimental study.
Results
We report findings from an experiment designed to test the effects of environmental variability on the adaptation and divergence of replicate populations of \textit{E. coli}. A total of 42 populations evolved for 2000 generations in 7 environmental regimes that differed in the number, identity, and presentation of the limiting resource. Regimes were organized in two sets, having the sugars glucose and maltose singly and in combination, or glucose and lactose singly and in combination. Combinations of sugars were presented either simultaneously or as temporally fluctuating resource regimes. This design allowed us to compare the effects of resource identity and presentation on the evolutionary trajectories followed by replicate populations. After 2000 generations, the fitness of all populations had increased relative to the common ancestor, but to different extents. Populations evolved in glucose improved the least, whereas populations evolving in maltose or lactose increased the most in their respective sets. Among-population divergence also differed across regimes, with variation higher in those groups that evolved in fluctuating environments than in those that faced constant resource regimens. This divergence under the fluctuating conditions increased between 1000 and 2000 generations, consistent with replicate populations evolving toward distinct adaptive peaks.
Conclusions
These results support the hypothesis that environmental heterogeneity can give rise to more rugged adaptive landscapes, which in turn promote evolutionary diversification. These results also demonstrate that this effect depends on the form of environmental heterogeneity, with greater divergence when the pairs of resources fluctuated temporally rather than being presented simultaneously.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Background
Environmental conditions affect the topology of the adaptive landscape and thus the trajectories followed by evolving populations. For example, a heterogeneous environment might lead to a more rugged adaptive landscape, making it more likely that replicate populations would evolve toward distinct adaptive peaks, relative to a uniform environment. To date, the influence of environmental variability on evolutionary dynamics has received relatively little experimental study.
Results
We report findings from an experiment designed to test the effects of environmental variability on the adaptation and divergence of replicate populations of E. coli. A total of 42 populations evolved for 2000 generations in 7 environmental regimes that differed in the number, identity, and presentation of the limiting resource. Regimes were organized in two sets, having the sugars glucose and maltose singly and in combination, or glucose and lactose singly and in combination. Combinations of sugars were presented either simultaneously or as temporally fluctuating resource regimes. This design allowed us to compare the effects of resource identity and presentation on the evolutionary trajectories followed by replicate populations. After 2000 generations, the fitness of all populations had increased relative to the common ancestor, but to different extents. Populations evolved in glucose improved the least, whereas populations evolving in maltose or lactose increased the most in their respective sets. Among-population divergence also differed across regimes, with variation higher in those groups that evolved in fluctuating environments than in those that faced constant resource regimens. This divergence under the fluctuating conditions increased between 1000 and 2000 generations, consistent with replicate populations evolving toward distinct adaptive peaks.
Conclusions
These results support the hypothesis that environmental heterogeneity can give rise to more rugged adaptive landscapes, which in turn promote evolutionary diversification. These results also demonstrate that this effect depends on the form of environmental heterogeneity, with greater divergence when the pairs of resources fluctuated temporally rather than being presented simultaneously.
Environmental conditions affect the topology of the adaptive landscape and thus the trajectories followed by evolving populations. For example, a heterogeneous environment might lead to a more rugged adaptive landscape, making it more likely that replicate populations would evolve toward distinct adaptive peaks, relative to a uniform environment. To date, the influence of environmental variability on evolutionary dynamics has received relatively little experimental study.
Results
We report findings from an experiment designed to test the effects of environmental variability on the adaptation and divergence of replicate populations of E. coli. A total of 42 populations evolved for 2000 generations in 7 environmental regimes that differed in the number, identity, and presentation of the limiting resource. Regimes were organized in two sets, having the sugars glucose and maltose singly and in combination, or glucose and lactose singly and in combination. Combinations of sugars were presented either simultaneously or as temporally fluctuating resource regimes. This design allowed us to compare the effects of resource identity and presentation on the evolutionary trajectories followed by replicate populations. After 2000 generations, the fitness of all populations had increased relative to the common ancestor, but to different extents. Populations evolved in glucose improved the least, whereas populations evolving in maltose or lactose increased the most in their respective sets. Among-population divergence also differed across regimes, with variation higher in those groups that evolved in fluctuating environments than in those that faced constant resource regimens. This divergence under the fluctuating conditions increased between 1000 and 2000 generations, consistent with replicate populations evolving toward distinct adaptive peaks.
Conclusions
These results support the hypothesis that environmental heterogeneity can give rise to more rugged adaptive landscapes, which in turn promote evolutionary diversification. These results also demonstrate that this effect depends on the form of environmental heterogeneity, with greater divergence when the pairs of resources fluctuated temporally rather than being presented simultaneously.
2008
Sleight S C; Orlic C; Schneider D; Lenski R E
Genetic Basis of Evolutionary Adaptation by Escherichia coli to Stressful Cycles of Freezing, Thawing and Growth Journal Article
Genetics, 180 (1), pp. 431–443, 2008, ISSN: 1943-2631.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Sleight2008,
title = {Genetic Basis of Evolutionary Adaptation by \textit{Escherichia coli} to Stressful Cycles of Freezing, Thawing and Growth},
author = {Sean C. Sleight and Christian Orlic and Dominique Schneider and Richard E. Lenski},
url = {https://academic.oup.com/genetics/article/180/1/431/6105123},
doi = {10.1534/genetics.108.091330},
issn = {1943-2631},
year = {2008},
date = {2008-09-01},
urldate = {2008-09-01},
journal = {Genetics},
volume = {180},
number = {1},
pages = {431--443},
abstract = {Microbial evolution experiments offer a powerful approach for coupling changes in complex phenotypes, including fitness and its components, with specific mutations. Here we investigate mutations substituted in 15 lines of \textit{Escherichia coli} that evolved for 1000 generations under freeze–thaw–growth (FTG) conditions. To investigate the genetic basis of their improvements, we screened many of the lines for mutations involving insertion sequence (IS) elements and identified two genes where multiple lines had similar mutations. Three lines had IS\textit{150} insertions in \textit{cls}, which encodes cardiolipin synthase, and 8 lines had IS\textit{150} insertions in the \textit{uspA-uspB} intergenic region, encoding two universal stress proteins. Another line had an 11-bp deletion mutation in the \textit{cls} gene. Strain reconstructions and competitions demonstrated that this deletion is beneficial under the FTG regime in its evolved genetic background. Further experiments showed that this \textit{cls} mutation helps maintain membrane fluidity after freezing and thawing and improves freeze–thaw (FT) survival. Reconstruction of isogenic strains also showed that the IS\textit{150} insertions in \textit{uspA/B} are beneficial under the FTG regime. The evolved insertions reduce \textit{uspB} transcription and increase both FT survival and recovery, but the physiological mechanism for this fitness improvement remains unknown.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Microbial evolution experiments offer a powerful approach for coupling changes in complex phenotypes, including fitness and its components, with specific mutations. Here we investigate mutations substituted in 15 lines of Escherichia coli that evolved for 1000 generations under freeze–thaw–growth (FTG) conditions. To investigate the genetic basis of their improvements, we screened many of the lines for mutations involving insertion sequence (IS) elements and identified two genes where multiple lines had similar mutations. Three lines had IS150 insertions in cls, which encodes cardiolipin synthase, and 8 lines had IS150 insertions in the uspA-uspB intergenic region, encoding two universal stress proteins. Another line had an 11-bp deletion mutation in the cls gene. Strain reconstructions and competitions demonstrated that this deletion is beneficial under the FTG regime in its evolved genetic background. Further experiments showed that this cls mutation helps maintain membrane fluidity after freezing and thawing and improves freeze–thaw (FT) survival. Reconstruction of isogenic strains also showed that the IS150 insertions in uspA/B are beneficial under the FTG regime. The evolved insertions reduce uspB transcription and increase both FT survival and recovery, but the physiological mechanism for this fitness improvement remains unknown.
Ostrowski E A; Woods R J; Lenski R E
The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli Journal Article
Proceedings of the Royal Society B: Biological Sciences, 275 (1632), pp. 277–284, 2008, ISSN: 0962-8452.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments, Genotypes and Phenotypes
@article{Ostrowski2008,
title = {The genetic basis of parallel and divergent phenotypic responses in evolving populations of \textit{Escherichia coli}},
author = {Elizabeth A. Ostrowski and Robert J. Woods and Richard E. Lenski},
url = {https://royalsocietypublishing.org/doi/10.1098/rspb.2007.1244},
doi = {10.1098/rspb.2007.1244},
issn = {0962-8452},
year = {2008},
date = {2008-02-01},
urldate = {2008-02-01},
journal = {Proceedings of the Royal Society B: Biological Sciences},
volume = {275},
number = {1632},
pages = {277--284},
abstract = {Pleiotropy plays a central role in theories of adaptation, but little is known about the distribution of pleiotropic effects associated with different adaptive mutations. Previously, we described the phenotypic effects of a collection of independently arising beneficial mutations in \textit{Escherichia coli}. We quantified their fitness effects in the glucose environment in which they evolved and their pleiotropic effects in five novel resource environments. Here we use a candidate gene approach to associate the phenotypic effects of the mutations with the underlying genetic changes. Among our collection of 27 adaptive mutants, we identified a total of 21 mutations (18 of which were unique) encompassing five different loci or gene regions. There was limited resolution to distinguish among loci based on their fitness effects in the glucose environment, demonstrating widespread parallelism in the direct response to selection. However, substantial heterogeneity in mutant effects was revealed when we examined their pleiotropic effects on fitness in the five novel environments. Substitutions in the same locus clustered together phenotypically, indicating concordance between molecular and phenotypic measures of divergence.},
keywords = {Descendant Experiments, Genotypes and Phenotypes},
pubstate = {published},
tppubtype = {article}
}
Pleiotropy plays a central role in theories of adaptation, but little is known about the distribution of pleiotropic effects associated with different adaptive mutations. Previously, we described the phenotypic effects of a collection of independently arising beneficial mutations in Escherichia coli. We quantified their fitness effects in the glucose environment in which they evolved and their pleiotropic effects in five novel resource environments. Here we use a candidate gene approach to associate the phenotypic effects of the mutations with the underlying genetic changes. Among our collection of 27 adaptive mutants, we identified a total of 21 mutations (18 of which were unique) encompassing five different loci or gene regions. There was limited resolution to distinguish among loci based on their fitness effects in the glucose environment, demonstrating widespread parallelism in the direct response to selection. However, substantial heterogeneity in mutant effects was revealed when we examined their pleiotropic effects on fitness in the five novel environments. Substitutions in the same locus clustered together phenotypically, indicating concordance between molecular and phenotypic measures of divergence.
2007
Bennett A F; Lenski R E
An experimental test of evolutionary trade-offs during temperature adaptation Journal Article
Proceedings of the National Academy of Sciences of the United States of America, 104 (Supplement 1), pp. 8649–8654, 2007, ISSN: 0027-8424.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Bennett2007,
title = {An experimental test of evolutionary trade-offs during temperature adaptation},
author = {Albert F. Bennett and Richard E. Lenski},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.0702117104},
doi = {10.1073/pnas.0702117104},
issn = {0027-8424},
year = {2007},
date = {2007-05-01},
urldate = {2007-05-01},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
volume = {104},
number = {Supplement 1},
pages = {8649--8654},
abstract = {We used experimental evolution to test directly the important and commonplace evolutionary hypothesis that adaptation, increased fitness within the selective environment, is accompanied by trade-off, a loss of fitness in other nonselective environments. Specifically, we determined whether trade-offs at high temperature generally and necessarily accompany genetic adaptation to low temperature. We measured the relative fitness increment of 24 lineages of the bacterium \textit{Escherichia coli} evolved for 2,000 generations at 20°C and the relative fitness decrement of these lines at 40°C. Trade-offs at the higher temperature were examined for their generality, universality, quantitative relationship, and historical contingency. Considering all 24 lines as a group, a significant decline in fitness was found at 40°C (mean decline = 9.4%), indicating the generality of the trade-off effect. However, in a lineage-by-lineage analysis, only 15 of 24 showed a significant trade-off, and one lineage increased fitness at high temperature. Thus, although general, trade-offs were not universal. Furthermore, there was no quantitative association between the magnitude of adaptive fitness increment at 20°C and fitness decline at 40°C, and no effect of lineages' historical thermal environment on either their improvement at 20°C or the extent of their trade-off at high temperature. We do not yet know the underlying mechanisms responsible for the trade-off, but they are sufficiently prevalent to drive a general effect. However, approximately one-third of the experimental lineages achieved low-temperature adaptation without detectable high-temperature trade-offs; therefore, it cannot be necessary that every change conferring benefit in cold environments has a negative effect on function in warmer environments.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
We used experimental evolution to test directly the important and commonplace evolutionary hypothesis that adaptation, increased fitness within the selective environment, is accompanied by trade-off, a loss of fitness in other nonselective environments. Specifically, we determined whether trade-offs at high temperature generally and necessarily accompany genetic adaptation to low temperature. We measured the relative fitness increment of 24 lineages of the bacterium Escherichia coli evolved for 2,000 generations at 20°C and the relative fitness decrement of these lines at 40°C. Trade-offs at the higher temperature were examined for their generality, universality, quantitative relationship, and historical contingency. Considering all 24 lines as a group, a significant decline in fitness was found at 40°C (mean decline = 9.4%), indicating the generality of the trade-off effect. However, in a lineage-by-lineage analysis, only 15 of 24 showed a significant trade-off, and one lineage increased fitness at high temperature. Thus, although general, trade-offs were not universal. Furthermore, there was no quantitative association between the magnitude of adaptive fitness increment at 20°C and fitness decline at 40°C, and no effect of lineages' historical thermal environment on either their improvement at 20°C or the extent of their trade-off at high temperature. We do not yet know the underlying mechanisms responsible for the trade-off, but they are sufficiently prevalent to drive a general effect. However, approximately one-third of the experimental lineages achieved low-temperature adaptation without detectable high-temperature trade-offs; therefore, it cannot be necessary that every change conferring benefit in cold environments has a negative effect on function in warmer environments.
Sleight S C; Lenski R E
Evolutionary Adaptation to Freeze‐Thaw‐Growth Cycles in Escherichia coli Journal Article
Physiological and Biochemical Zoology, 80 (4), pp. 370 - 385, 2007, ISSN: 1522-2152.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{nokey,
title = {Evolutionary Adaptation to Freeze‐Thaw‐Growth Cycles in \textit{Escherichia coli}},
author = {Sean C. Sleight and Richard E. Lenski},
url = {https://www.journals.uchicago.edu/doi/10.1086/518013},
doi = {10.1086/518013},
issn = {1522-2152},
year = {2007},
date = {2007-02-13},
urldate = {2007-02-13},
journal = {Physiological and Biochemical Zoology},
volume = {80},
number = {4},
pages = {370 - 385},
abstract = {Fifteen populations of \textit{Escherichia coli} were propagated for 150 freeze‐thaw‐growth (FTG) cycles in order to study the phenotypic and genetic changes that evolve under these stressful conditions. Here we present the phenotypic differences between the evolved lines and their progenitors as measured by competition experiments and growth curves. Three FTG lines evolved from an ancestral strain that was previously used to start a long‐term evolution experiment, while the other 12 FTG lines are derived from clones that had previously evolved for 20,000 generations at constant 37°C. Competition experiments indicate that the former FTG group improved their mean fitness under the FTG regime by about 90% relative to their progenitor, while the latter FTG group gained on average about 60% relative to their own progenitors. These increases in fitness result from both improved survival during freezing and thawing and more rapid recovery to initiate exponential growth after thawing. This shorter lag phase is specific to recovery after freezing and thawing. Future work will seek to identify the mutations responsible for evolutionary adaptation to the FTG environment and use them to explore the physiological mechanisms that allow increased survival and more rapid recovery.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Fifteen populations of Escherichia coli were propagated for 150 freeze‐thaw‐growth (FTG) cycles in order to study the phenotypic and genetic changes that evolve under these stressful conditions. Here we present the phenotypic differences between the evolved lines and their progenitors as measured by competition experiments and growth curves. Three FTG lines evolved from an ancestral strain that was previously used to start a long‐term evolution experiment, while the other 12 FTG lines are derived from clones that had previously evolved for 20,000 generations at constant 37°C. Competition experiments indicate that the former FTG group improved their mean fitness under the FTG regime by about 90% relative to their progenitor, while the latter FTG group gained on average about 60% relative to their own progenitors. These increases in fitness result from both improved survival during freezing and thawing and more rapid recovery to initiate exponential growth after thawing. This shorter lag phase is specific to recovery after freezing and thawing. Future work will seek to identify the mutations responsible for evolutionary adaptation to the FTG environment and use them to explore the physiological mechanisms that allow increased survival and more rapid recovery.
Cooper T F
Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli Journal Article
PLoS Biology, 5 (9), pp. e225, 2007.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments, Fitness Trajectories
@article{Cooper2007,
title = {Recombination speeds adaptation by reducing competition between beneficial mutations in populations of \textit{Escherichia coli}},
author = {Tim F. Cooper},
doi = {10.1371/journal.pbio.0050225},
year = {2007},
date = {2007-01-01},
urldate = {2007-01-01},
journal = {PLoS Biology},
volume = {5},
number = {9},
pages = {e225},
abstract = {Identification of the selective forces contributing to the origin and maintenance of sex is a fundamental problem in biology. The Fisher-Muller model proposes that sex is advantageous because it allows beneficial mutations that arise in different lineages to recombine, thereby reducing clonal interference and speeding adaptation. I used the F plasmid to mediate recombination in the bacterium \textit{Escherichia coli} and measured its effect on adaptation at high and low mutation rates. Recombination increased the rate of adaptation approximately 3-fold more in the high mutation rate treatment, where beneficial mutations had to compete for fixation. Sequencing of candidate loci revealed the presence of a beneficial mutation in six high mutation rate lines. In the absence of recombination, this mutation took longer to fix and, over the course of its substitution, conferred a reduced competitive advantage, indicating interference between competing beneficial mutations. Together, these results provide experimental support for the Fisher-Muller model and demonstrate that plasmid-mediated gene transfer can accelerate bacterial adaptation.},
keywords = {Descendant Experiments, Fitness Trajectories},
pubstate = {published},
tppubtype = {article}
}
Identification of the selective forces contributing to the origin and maintenance of sex is a fundamental problem in biology. The Fisher-Muller model proposes that sex is advantageous because it allows beneficial mutations that arise in different lineages to recombine, thereby reducing clonal interference and speeding adaptation. I used the F plasmid to mediate recombination in the bacterium Escherichia coli and measured its effect on adaptation at high and low mutation rates. Recombination increased the rate of adaptation approximately 3-fold more in the high mutation rate treatment, where beneficial mutations had to compete for fixation. Sequencing of candidate loci revealed the presence of a beneficial mutation in six high mutation rate lines. In the absence of recombination, this mutation took longer to fix and, over the course of its substitution, conferred a reduced competitive advantage, indicating interference between competing beneficial mutations. Together, these results provide experimental support for the Fisher-Muller model and demonstrate that plasmid-mediated gene transfer can accelerate bacterial adaptation.
Beerenwinkel N; Pachter L; Sturmfels B; Elena S F; Lenski R E
Analysis of epistatic interactions and fitness landscapes using a new geometric approach Journal Article
BMC Evolutionary Biology, 7 (1), pp. 60, 2007, ISSN: 14712148.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Beerenwinkel2007,
title = {Analysis of epistatic interactions and fitness landscapes using a new geometric approach},
author = {Niko Beerenwinkel and Lior Pachter and Bernd Sturmfels and Santiago F. Elena and Richard E. Lenski},
url = {http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-7-60},
doi = {10.1186/1471-2148-7-60},
issn = {14712148},
year = {2007},
date = {2007-01-01},
urldate = {2007-01-01},
journal = {BMC Evolutionary Biology},
volume = {7},
number = {1},
pages = {60},
abstract = {Background
Understanding interactions between mutations and how they affect fitness is a central problem in evolutionary biology that bears on such fundamental issues as the structure of fitness landscapes and the evolution of sex. To date, analyses of fitness landscapes have focused either on the overall directional curvature of the fitness landscape or on the distribution of pairwise interactions. In this paper, we propose and employ a new mathematical approach that allows a more complete description of multi-way interactions and provides new insights into the structure of fitness landscapes.
Results
We apply the mathematical theory of gene interactions developed by Beerenwinkel et al. to a fitness landscape for \textit{Escherichia coli} obtained by Elena and Lenski. The genotypes were constructed by introducing nine mutations into a wild-type strain and constructing a restricted set of 27 double mutants. Despite the absence of mutants higher than second order, our analysis of this genotypic space points to previously unappreciated gene interactions, in addition to the standard pairwise epistasis. Our analysis confirms Elena and Lenski's inference that the fitness landscape is complex, so that an overall measure of curvature obscures a diversity of interaction types. We also demonstrate that some mutations contribute disproportionately to this complexity. In particular, some mutations are systematically better than others at mixing with other mutations. We also find a strong correlation between epistasis and the average fitness loss caused by deleterious mutations. In particular, the epistatic deviations from multiplicative expectations tend toward more positive values in the context of more deleterious mutations, emphasizing that pairwise epistasis is a local property of the fitness landscape. Finally, we determine the geometry of the fitness landscape, which reflects many of these biologically interesting features.
Conclusion
A full description of complex fitness landscapes requires more information than the average curvature or the distribution of independent pairwise interactions. We have proposed a mathematical approach that, in principle, allows a complete description and, in practice, can suggest new insights into the structure of real fitness landscapes. Our analysis emphasizes the value of non-independent genotypes for these inferences.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Background
Understanding interactions between mutations and how they affect fitness is a central problem in evolutionary biology that bears on such fundamental issues as the structure of fitness landscapes and the evolution of sex. To date, analyses of fitness landscapes have focused either on the overall directional curvature of the fitness landscape or on the distribution of pairwise interactions. In this paper, we propose and employ a new mathematical approach that allows a more complete description of multi-way interactions and provides new insights into the structure of fitness landscapes.
Results
We apply the mathematical theory of gene interactions developed by Beerenwinkel et al. to a fitness landscape for Escherichia coli obtained by Elena and Lenski. The genotypes were constructed by introducing nine mutations into a wild-type strain and constructing a restricted set of 27 double mutants. Despite the absence of mutants higher than second order, our analysis of this genotypic space points to previously unappreciated gene interactions, in addition to the standard pairwise epistasis. Our analysis confirms Elena and Lenski's inference that the fitness landscape is complex, so that an overall measure of curvature obscures a diversity of interaction types. We also demonstrate that some mutations contribute disproportionately to this complexity. In particular, some mutations are systematically better than others at mixing with other mutations. We also find a strong correlation between epistasis and the average fitness loss caused by deleterious mutations. In particular, the epistatic deviations from multiplicative expectations tend toward more positive values in the context of more deleterious mutations, emphasizing that pairwise epistasis is a local property of the fitness landscape. Finally, we determine the geometry of the fitness landscape, which reflects many of these biologically interesting features.
Conclusion
A full description of complex fitness landscapes requires more information than the average curvature or the distribution of independent pairwise interactions. We have proposed a mathematical approach that, in principle, allows a complete description and, in practice, can suggest new insights into the structure of real fitness landscapes. Our analysis emphasizes the value of non-independent genotypes for these inferences.
Understanding interactions between mutations and how they affect fitness is a central problem in evolutionary biology that bears on such fundamental issues as the structure of fitness landscapes and the evolution of sex. To date, analyses of fitness landscapes have focused either on the overall directional curvature of the fitness landscape or on the distribution of pairwise interactions. In this paper, we propose and employ a new mathematical approach that allows a more complete description of multi-way interactions and provides new insights into the structure of fitness landscapes.
Results
We apply the mathematical theory of gene interactions developed by Beerenwinkel et al. to a fitness landscape for Escherichia coli obtained by Elena and Lenski. The genotypes were constructed by introducing nine mutations into a wild-type strain and constructing a restricted set of 27 double mutants. Despite the absence of mutants higher than second order, our analysis of this genotypic space points to previously unappreciated gene interactions, in addition to the standard pairwise epistasis. Our analysis confirms Elena and Lenski's inference that the fitness landscape is complex, so that an overall measure of curvature obscures a diversity of interaction types. We also demonstrate that some mutations contribute disproportionately to this complexity. In particular, some mutations are systematically better than others at mixing with other mutations. We also find a strong correlation between epistasis and the average fitness loss caused by deleterious mutations. In particular, the epistatic deviations from multiplicative expectations tend toward more positive values in the context of more deleterious mutations, emphasizing that pairwise epistasis is a local property of the fitness landscape. Finally, we determine the geometry of the fitness landscape, which reflects many of these biologically interesting features.
Conclusion
A full description of complex fitness landscapes requires more information than the average curvature or the distribution of independent pairwise interactions. We have proposed a mathematical approach that, in principle, allows a complete description and, in practice, can suggest new insights into the structure of real fitness landscapes. Our analysis emphasizes the value of non-independent genotypes for these inferences.
2005
Ostrowski E A; Rozen D E; Lenski R E
Pleiotropic effects of beneficial mutations in Escherichia coli Journal Article
Evolution, 59 (11), pp. 2343–2352, 2005, ISSN: 0014-3820.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Descendant Experiments
@article{Ostrowski2005,
title = {Pleiotropic effects of beneficial mutations in \textit{Escherichia coli}},
author = {Elizabeth A. Ostrowski and Daniel E. Rozen and Richard E. Lenski},
url = {https://onlinelibrary.wiley.com/doi/10.1111/j.0014-3820.2005.tb00944.x},
doi = {10.1111/j.0014-3820.2005.tb00944.x},
issn = {0014-3820},
year = {2005},
date = {2005-11-01},
urldate = {2005-11-01},
journal = {Evolution},
volume = {59},
number = {11},
pages = {2343--2352},
abstract = {Micromutational models of adaptation have placed considerable weight on antagonistic pleiotropy as a mechanism that prevents mutations of large effect from achieving fixation. However, there are few empirical studies of the distribution of pleiotropic effects, and no studies that have examined this distribution for a large number of adaptive mutations. Here we examine the form and extent of pleiotropy associated with beneficial mutations in \textit{Escherichia coli}. To do so, we used a collection of independently evolved genotypes, each of which contains a beneficial mutation that confers increased fitness in a glucose-limited environment. To determine the pleiotropic effects of these mutations, we examined the fitnesses of the mutants in five novel resource environments. Our results show that the majority of mutations had significant fitness effects in alternative resources, such that pleiotropy was common. The predominant form of this pleiotropy was positive - that is, most mutations that conferred increased fitness in glucose also conferred increased fitness in novel resources. We did detect some deleterious pleiotropic effects, but they were primarily limited to one of the five resources, and within this resource, to only a subset of mutants. Although pleiotropic effects were generally positive, fitness levels were lower and more variable on resources that differed most in their mechanisms of uptake and catabolism from that of glucose. Positive pleiotropic effects were strongly correlated in magnitude with their direct effects, but no such correlation was found among mutants with deleterious pleiotropic effects. Whereas previous studies of populations evolved on glucose for longer periods of time showed consistent declines on some of the resources used here, our results suggest that deleterious pleiotropic effects were limited to only a subset of the beneficial mutations available. },
keywords = {Correlated Responses, Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Micromutational models of adaptation have placed considerable weight on antagonistic pleiotropy as a mechanism that prevents mutations of large effect from achieving fixation. However, there are few empirical studies of the distribution of pleiotropic effects, and no studies that have examined this distribution for a large number of adaptive mutations. Here we examine the form and extent of pleiotropy associated with beneficial mutations in Escherichia coli. To do so, we used a collection of independently evolved genotypes, each of which contains a beneficial mutation that confers increased fitness in a glucose-limited environment. To determine the pleiotropic effects of these mutations, we examined the fitnesses of the mutants in five novel resource environments. Our results show that the majority of mutations had significant fitness effects in alternative resources, such that pleiotropy was common. The predominant form of this pleiotropy was positive - that is, most mutations that conferred increased fitness in glucose also conferred increased fitness in novel resources. We did detect some deleterious pleiotropic effects, but they were primarily limited to one of the five resources, and within this resource, to only a subset of mutants. Although pleiotropic effects were generally positive, fitness levels were lower and more variable on resources that differed most in their mechanisms of uptake and catabolism from that of glucose. Positive pleiotropic effects were strongly correlated in magnitude with their direct effects, but no such correlation was found among mutants with deleterious pleiotropic effects. Whereas previous studies of populations evolved on glucose for longer periods of time showed consistent declines on some of the resources used here, our results suggest that deleterious pleiotropic effects were limited to only a subset of the beneficial mutations available.
2004
Remold S K; Lenski R E
Pervasive joint influence of epistasis and plasticity on mutational effects in Escherichia coli Journal Article
Nature Genetics, 36 (4), pp. 423–426, 2004, ISSN: 1061-4036.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Remold2004,
title = {Pervasive joint influence of epistasis and plasticity on mutational effects in \textit{Escherichia coli}},
author = {Susanna K. Remold and Richard E. Lenski},
url = {http://www.nature.com/articles/ng1324},
doi = {10.1038/ng1324},
issn = {1061-4036},
year = {2004},
date = {2004-04-01},
urldate = {2004-04-01},
journal = {Nature Genetics},
volume = {36},
number = {4},
pages = {423--426},
abstract = {The effects of mutations on phenotype and fitness may depend on the environment (phenotypic plasticity), other mutations (genetic epistasis) or both. Here we examine the fitness effects of 18 random insertion mutations in \textit{E. coli} in two resource environments and five genetic backgrounds. We tested each mutation for plasticity and epistasis by comparing its fitness effects across these ecological and genetic contexts. Some mutations had no measurable effect in any of these contexts. None of the mutations had effects on phenotypic plasticity that were independent of genetic background. However, half the mutations had epistatic interactions such that their effects differed among genetic backgrounds, usually in an environment-dependent manner. Also, the pattern of mutational effects across backgrounds indicated that epistasis had been shaped primarily by unique events in the evolutionary history of a population rather than by repeatable events associated with shared environmental history.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
The effects of mutations on phenotype and fitness may depend on the environment (phenotypic plasticity), other mutations (genetic epistasis) or both. Here we examine the fitness effects of 18 random insertion mutations in E. coli in two resource environments and five genetic backgrounds. We tested each mutation for plasticity and epistasis by comparing its fitness effects across these ecological and genetic contexts. Some mutations had no measurable effect in any of these contexts. None of the mutations had effects on phenotypic plasticity that were independent of genetic background. However, half the mutations had epistatic interactions such that their effects differed among genetic backgrounds, usually in an environment-dependent manner. Also, the pattern of mutational effects across backgrounds indicated that epistasis had been shaped primarily by unique events in the evolutionary history of a population rather than by repeatable events associated with shared environmental history.
2003
Riehle M M; Bennett A F; Lenski R E; Long A D
Evolutionary changes in heat-inducible gene expression in lines of Escherichia coli adapted to high temperature Journal Article
Physiological Genomics, 14 (1), pp. 47–58, 2003, ISSN: 1094-8341.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Riehle2003,
title = {Evolutionary changes in heat-inducible gene expression in lines of \textit{Escherichia coli} adapted to high temperature},
author = {Michelle M. Riehle and Albert F. Bennett and Richard E. Lenski and Anthony D. Long},
url = {https://www.physiology.org/doi/10.1152/physiolgenomics.00034.2002},
doi = {10.1152/physiolgenomics.00034.2002},
issn = {1094-8341},
year = {2003},
date = {2003-06-01},
urldate = {2003-06-01},
journal = {Physiological Genomics},
volume = {14},
number = {1},
pages = {47--58},
abstract = {The involvement of heat-inducible genes, including the heat-shock genes, in the acute response to temperature stress is well established. However, their importance in genetic adaptation to long-term temperature stress is less clear. Here we use high-density arrays to examine changes in expression for 35 heat-inducible genes in three independent lines of \textit{Escherichia coli} that evolved at high temperature (41.5°C) for 2,000 generations. These lines exhibited significant changes in heat-inducible gene expression relative to their ancestor, including parallel changes in \textit{fkpA}, \textit{gapA}, and \textit{hslT}. As a group, the heat-inducible genes were significantly more likely than noncandidate genes to have evolved changes in expression. Genes encoding molecular chaperones and ATP-dependent proteases, key components of the cytoplasmic stress response, exhibit relatively little expression change; whereas genes with periplasmic functions exhibit significant expression changes suggesting a key role for the extracytoplasmic stress response in the adaptation to high temperature. Following acclimation at 41.5°C, two of the three lines exhibited significantly improved survival at 50°C, indicating changes in inducible thermotolerance. Thus evolution at high temperature led to significant changes at the molecular level in heat-inducible gene expression and at the organismal level in inducible thermotolerance and fitness.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
The involvement of heat-inducible genes, including the heat-shock genes, in the acute response to temperature stress is well established. However, their importance in genetic adaptation to long-term temperature stress is less clear. Here we use high-density arrays to examine changes in expression for 35 heat-inducible genes in three independent lines of Escherichia coli that evolved at high temperature (41.5°C) for 2,000 generations. These lines exhibited significant changes in heat-inducible gene expression relative to their ancestor, including parallel changes in fkpA, gapA, and hslT. As a group, the heat-inducible genes were significantly more likely than noncandidate genes to have evolved changes in expression. Genes encoding molecular chaperones and ATP-dependent proteases, key components of the cytoplasmic stress response, exhibit relatively little expression change; whereas genes with periplasmic functions exhibit significant expression changes suggesting a key role for the extracytoplasmic stress response in the adaptation to high temperature. Following acclimation at 41.5°C, two of the three lines exhibited significantly improved survival at 50°C, indicating changes in inducible thermotolerance. Thus evolution at high temperature led to significant changes at the molecular level in heat-inducible gene expression and at the organismal level in inducible thermotolerance and fitness.
2001
Cullum A J; Bennett A F; Lenski R E
Evolutionary adaptation to temperature. IX. Preadaptation to novel stressful environments of Escherichia coli adapted to high temperature Journal Article
Evolution, 55 (11), pp. 2194–2202, 2001, ISSN: 0014-3820.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Cullum2001,
title = {Evolutionary adaptation to temperature. IX. Preadaptation to novel stressful environments of \textit{Escherichia coli} adapted to high temperature},
author = {Alistair J. Cullum and Albert F. Bennett and Richard E. Lenski},
url = {https://onlinelibrary.wiley.com/doi/10.1111/j.0014-3820.2001.tb00735.x},
doi = {10.1111/j.0014-3820.2001.tb00735.x},
issn = {0014-3820},
year = {2001},
date = {2001-11-01},
urldate = {2001-11-01},
journal = {Evolution},
volume = {55},
number = {11},
pages = {2194--2202},
abstract = {Stressful environments may be considered as those that reduce fitness, sometimes due in part to the increased metabolic expenditure required to sustain life. Direct adaptation to a stressor is expected to increase fitness and reduce maintenance metabolism, with the latter leading to increased biomass production. In this study, we test the general hypothesis that such adaptation to one stressor can preadapt organisms to novel stressful environments. Six lines of \textit{Escherichia coli} propagated for 2000 generations at 41-42°C (42 group), a stressful temperature, were compared to six control lines propagated for 2000 generations at 37°C (37 group) and to the common ancestor of both groups. We assayed biovolume yield (a measure of growth efficiency) and competitive fitness in the 42 group's selective high temperature environment as well as five novel stressful environments - acid, alkali, ethanol, high osmolarity and peroxide. As previously reported, at high temperature the 42 group had both higher yield and fitness than the 37 group and ancestor. In the novel environments, the 42 group generally produced yields higher than the 37 group (and marginally higher than the ancestor), but we found no differences in competitive fitness among the 37 and 42 groups and the ancestor. We also found that the performance of lines within groups was not correlated across stressful environments for either yield or relative fitness. Because previous adaptation to one stressor did not improve our measure of Darwinian fitness in novel stressful environments, we conclude that the 42 group shows no useful pre-adaptation, or cross-tolerance, to these types of environments.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Stressful environments may be considered as those that reduce fitness, sometimes due in part to the increased metabolic expenditure required to sustain life. Direct adaptation to a stressor is expected to increase fitness and reduce maintenance metabolism, with the latter leading to increased biomass production. In this study, we test the general hypothesis that such adaptation to one stressor can preadapt organisms to novel stressful environments. Six lines of Escherichia coli propagated for 2000 generations at 41-42°C (42 group), a stressful temperature, were compared to six control lines propagated for 2000 generations at 37°C (37 group) and to the common ancestor of both groups. We assayed biovolume yield (a measure of growth efficiency) and competitive fitness in the 42 group's selective high temperature environment as well as five novel stressful environments - acid, alkali, ethanol, high osmolarity and peroxide. As previously reported, at high temperature the 42 group had both higher yield and fitness than the 37 group and ancestor. In the novel environments, the 42 group generally produced yields higher than the 37 group (and marginally higher than the ancestor), but we found no differences in competitive fitness among the 37 and 42 groups and the ancestor. We also found that the performance of lines within groups was not correlated across stressful environments for either yield or relative fitness. Because previous adaptation to one stressor did not improve our measure of Darwinian fitness in novel stressful environments, we conclude that the 42 group shows no useful pre-adaptation, or cross-tolerance, to these types of environments.
Remold S K; Lenski R E
Contribution of individual random mutations to genotype-by-environment interactions in Escherichia coli Journal Article
Proceedings of the National Academy of Sciences of the United States of America, 98 (20), pp. 11388–11393, 2001, ISSN: 0027-8424.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Remold2001,
title = {Contribution of individual random mutations to genotype-by-environment interactions in \textit{Escherichia coli}},
author = {Susanna K. Remold and Richard E. Lenski},
url = {http://www.pnas.org/cgi/doi/10.1073/pnas.201140198},
doi = {10.1073/pnas.201140198},
issn = {0027-8424},
year = {2001},
date = {2001-09-01},
urldate = {2001-09-01},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
volume = {98},
number = {20},
pages = {11388--11393},
abstract = {Numerous studies have shown genotype-by-environment (GxE) interactions for traits related to organismal fitness. However, the genetic architecture of the interaction is usually unknown because these studies used genotypes that differ from one another by many unknown mutations. These mutations were also present as standing variation in populations and hence had been subject to prior selection. Based on such studies, it is therefore impossible to say what fraction of new, random mutations contributes to GxE interactions. In this study, we measured the fitness in four environments of 26 genotypes of \textit{Escherichia coli}, each containing a single random insertion mutation. Fitness was measured relative to their common progenitor, which had evolved on glucose at 37°C for the preceding 10,000 generations. The four assay environments differed in limiting resource and temperature (glucose, 28°C; maltose, 28°C; glucose, 37°C; and maltose, 37°C). A highly significant interaction between mutation and resource was found. In contrast, there was no interaction involving temperature. The resource interaction reflected much higher among mutation variation for fitness in maltose than in glucose. At least 11 mutations (42%) contributed to this GxE interaction through their differential fitness effects across resources. Beneficial mutations are generally thought to be rare but, surprisingly, at least three mutations (12%) significantly improved fitness in maltose, a resource novel to the progenitor. More generally, our findings demonstrate that GxE interactions can be quite common, even for genotypes that differ by only one mutation and in environments differing by only a single factor.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Numerous studies have shown genotype-by-environment (GxE) interactions for traits related to organismal fitness. However, the genetic architecture of the interaction is usually unknown because these studies used genotypes that differ from one another by many unknown mutations. These mutations were also present as standing variation in populations and hence had been subject to prior selection. Based on such studies, it is therefore impossible to say what fraction of new, random mutations contributes to GxE interactions. In this study, we measured the fitness in four environments of 26 genotypes of Escherichia coli, each containing a single random insertion mutation. Fitness was measured relative to their common progenitor, which had evolved on glucose at 37°C for the preceding 10,000 generations. The four assay environments differed in limiting resource and temperature (glucose, 28°C; maltose, 28°C; glucose, 37°C; and maltose, 37°C). A highly significant interaction between mutation and resource was found. In contrast, there was no interaction involving temperature. The resource interaction reflected much higher among mutation variation for fitness in maltose than in glucose. At least 11 mutations (42%) contributed to this GxE interaction through their differential fitness effects across resources. Beneficial mutations are generally thought to be rare but, surprisingly, at least three mutations (12%) significantly improved fitness in maltose, a resource novel to the progenitor. More generally, our findings demonstrate that GxE interactions can be quite common, even for genotypes that differ by only one mutation and in environments differing by only a single factor.
2000
Moore F B G; Rozen D E; Lenski R E
Pervasive compensatory adaptation in Escherichia coli Journal Article
Proceedings of the Royal Society of London. Series B: Biological Sciences, 267 (1442), pp. 515–522, 2000, ISSN: 0962-8452.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Moore2000,
title = {Pervasive compensatory adaptation in \textit{Escherichia coli}},
author = {Francisco B. G. Moore and Daniel E. Rozen and Richard E. Lenski},
url = {https://royalsocietypublishing.org/doi/10.1098/rspb.2000.1030},
doi = {10.1098/rspb.2000.1030},
issn = {0962-8452},
year = {2000},
date = {2000-03-01},
urldate = {2000-03-01},
journal = {Proceedings of the Royal Society of London. Series B: Biological Sciences},
volume = {267},
number = {1442},
pages = {515--522},
abstract = {To investigate compensatory adaptation (CA), we used genotypes of \textit{Escherichia coli} which were identical except for one or two deleterious mutations. We compared CA for (i) deleterious mutations with large versus small effects, (ii) genotypes carrying one versus two mutations, and (iii) pairs of deleterious mutations which interact in a multiplicative versus synergistic fashion. In all, we studied 14 different genotypes, plus a control strain which was not mutated. Most genotypes showed CA during 200 generations of experimental evolution, where we define CA as a fitness increase which is disproportionately large relative to that in evolving control lines, coupled with retention of the original deleterious mutation(s). We observed greater CA for mutations of large effect than for those of small effect, which can be explained by the greater benefit to recovery in severely handicapped genotypes given the dynamics of selection. The rates of CA were similar for double and single mutants whose initial fitnesses were approximately equal. CA was faster for synergistic than for multiplicative pairs, presumably because the marginal gain which results from CA for one of the component mutations is greater in that case. The most surprising result in our view, is that compensation should be so readily achieved in an organism which is haploid and has little genetic redundancy. This finding suggests a degree of versatility in the \textit{E. coli} genome which demands further study from both genetic and physiological perspectives.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
To investigate compensatory adaptation (CA), we used genotypes of Escherichia coli which were identical except for one or two deleterious mutations. We compared CA for (i) deleterious mutations with large versus small effects, (ii) genotypes carrying one versus two mutations, and (iii) pairs of deleterious mutations which interact in a multiplicative versus synergistic fashion. In all, we studied 14 different genotypes, plus a control strain which was not mutated. Most genotypes showed CA during 200 generations of experimental evolution, where we define CA as a fitness increase which is disproportionately large relative to that in evolving control lines, coupled with retention of the original deleterious mutation(s). We observed greater CA for mutations of large effect than for those of small effect, which can be explained by the greater benefit to recovery in severely handicapped genotypes given the dynamics of selection. The rates of CA were similar for double and single mutants whose initial fitnesses were approximately equal. CA was faster for synergistic than for multiplicative pairs, presumably because the marginal gain which results from CA for one of the component mutations is greater in that case. The most surprising result in our view, is that compensation should be so readily achieved in an organism which is haploid and has little genetic redundancy. This finding suggests a degree of versatility in the E. coli genome which demands further study from both genetic and physiological perspectives.
1999
Mongold J A; Bennett A F; Lenski R E
Evolutionary adaptation to temperature. VII. Extension of the upper thermal limit of Escherichia coli Journal Article
Evolution, 53 (2), pp. 386–394, 1999, ISSN: 0014-3820.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Mongold1999,
title = {Evolutionary adaptation to temperature. VII. Extension of the upper thermal limit of \textit{Escherichia coli}},
author = {Judith A. Mongold and Albert F. Bennett and Richard E. Lenski},
url = {https://onlinelibrary.wiley.com/doi/10.1111/j.1558-5646.1999.tb03774.x},
doi = {10.1111/j.1558-5646.1999.tb03774.x},
issn = {0014-3820},
year = {1999},
date = {1999-04-01},
urldate = {1999-04-01},
journal = {Evolution},
volume = {53},
number = {2},
pages = {386--394},
abstract = {What factors influence the ability of populations to adapt to extreme environments that lie outside their current tolerance limits? We investigated this question by exposing experimental populations of the bacterium \textit{Escherichia coli} to lethally high temperatures. We asked: (1) whether we could obtain thermotolerant mutants with an extended upper thermal limit by this selective screen; (2) whether the propensity to obtain thermotolerant mutants depended on the prior selective history of the progenitor genotypes; and (3) how the fitness properties of these mutants compared to those of their progenitors within the ancestral thermal niche. Specifically, we subjected 15 independent populations founded from each of six progenitors to 44°C; all of the progenitors had upper thermal limits between about 40°C and 42°C. Two of the progenitors were from populations that had previously adapted to 32°C, two were from populations adapted to 37°C, and two were from populations adapted to 41-42°C. All 90 populations were screened for mutants that could survive and grow at 44°C. We obtained three thermotolerant mutants, all derived from progenitors previously adapted to 41-42°C. In an earlier study, we serendipitously found one other thermotolerant mutant derived from a population that had previously adapted to 32°C. Thus, prior selection at an elevated but nonlethal temperature may predispose organisms to evolve more extreme thermotolerance, but this is not an absolute requirement. It is evidently possible to obtain mutants that tolerate more extreme temperatures, so why did they not become prevalent during prior selection at 41-42°C, near the upper limit of the thermal niche? To address this question, we measured the fitness of the thermotolerant mutants at high temperatures just within the ancestral niche. None of the four thermotolerant mutants had an advantage relative to their progenitor even very near the upper limit of the thermal niche; in fact, all of the mutants showed a noticeable loss of fitness around 41°C. Thus, the genetic adaptations that improve competitive fitness at high but nonlethal temperatures are distinct from those that permit tolerance of otherwise lethal temperatures.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
What factors influence the ability of populations to adapt to extreme environments that lie outside their current tolerance limits? We investigated this question by exposing experimental populations of the bacterium Escherichia coli to lethally high temperatures. We asked: (1) whether we could obtain thermotolerant mutants with an extended upper thermal limit by this selective screen; (2) whether the propensity to obtain thermotolerant mutants depended on the prior selective history of the progenitor genotypes; and (3) how the fitness properties of these mutants compared to those of their progenitors within the ancestral thermal niche. Specifically, we subjected 15 independent populations founded from each of six progenitors to 44°C; all of the progenitors had upper thermal limits between about 40°C and 42°C. Two of the progenitors were from populations that had previously adapted to 32°C, two were from populations adapted to 37°C, and two were from populations adapted to 41-42°C. All 90 populations were screened for mutants that could survive and grow at 44°C. We obtained three thermotolerant mutants, all derived from progenitors previously adapted to 41-42°C. In an earlier study, we serendipitously found one other thermotolerant mutant derived from a population that had previously adapted to 32°C. Thus, prior selection at an elevated but nonlethal temperature may predispose organisms to evolve more extreme thermotolerance, but this is not an absolute requirement. It is evidently possible to obtain mutants that tolerate more extreme temperatures, so why did they not become prevalent during prior selection at 41-42°C, near the upper limit of the thermal niche? To address this question, we measured the fitness of the thermotolerant mutants at high temperatures just within the ancestral niche. None of the four thermotolerant mutants had an advantage relative to their progenitor even very near the upper limit of the thermal niche; in fact, all of the mutants showed a noticeable loss of fitness around 41°C. Thus, the genetic adaptations that improve competitive fitness at high but nonlethal temperatures are distinct from those that permit tolerance of otherwise lethal temperatures.
Bennett A F; Lenski R E
Experimental Evolution and Its Role in Evolutionary Physiology Journal Article
American Zoologist, 39 (2), pp. 346–362, 1999, ISSN: 0003-1569.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{10.1093/icb/39.2.346,
title = {Experimental Evolution and Its Role in Evolutionary Physiology},
author = {Albert F. Bennett and Richard E. Lenski},
url = {https://doi.org/10.1093/icb/39.2.346
https://academic.oup.com/icb/article-lookup/doi/10.1093/icb/39.2.346},
doi = {10.1093/icb/39.2.346},
issn = {0003-1569},
year = {1999},
date = {1999-04-01},
urldate = {1999-04-01},
journal = {American Zoologist},
volume = {39},
number = {2},
pages = {346--362},
abstract = {Four general approaches to the study of evolutionary physiology—phylogenetically-based comparisons, genetic analyses and manipulations, phenotypic plasticity and manipulation, and selection studies—are outlined and discussed. We provide an example of the latter, the application of laboratory selection experiments to the study of a general issue in environmental adaptation, differences in adaptive patterns of generalists and specialists. A clone of the bacterium \textit{Escherichia coli} that had evolved in a constant environment of 37°C was replicated into 6 populations and allowed to reproduce for 2,000 generations in a variable thermal environment alternating between 32 and 42°C. As predicted by theory, fitness and efficiency of resource use increased in this new environment, as did stress resistance. Contrary to predictions, however, fitness and efficiency in the constant ancestral environment of 37°C did not decrease, nor did thermal niche breadth or phenotypic plasticity increase. Selection experiments can thus provide a valuable approach to testing hypotheses and assumptions about the evolution of functional characters.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Four general approaches to the study of evolutionary physiology—phylogenetically-based comparisons, genetic analyses and manipulations, phenotypic plasticity and manipulation, and selection studies—are outlined and discussed. We provide an example of the latter, the application of laboratory selection experiments to the study of a general issue in environmental adaptation, differences in adaptive patterns of generalists and specialists. A clone of the bacterium Escherichia coli that had evolved in a constant environment of 37°C was replicated into 6 populations and allowed to reproduce for 2,000 generations in a variable thermal environment alternating between 32 and 42°C. As predicted by theory, fitness and efficiency of resource use increased in this new environment, as did stress resistance. Contrary to predictions, however, fitness and efficiency in the constant ancestral environment of 37°C did not decrease, nor did thermal niche breadth or phenotypic plasticity increase. Selection experiments can thus provide a valuable approach to testing hypotheses and assumptions about the evolution of functional characters.
Vasi F K; Lenski R E
Ecological strategies and fitness tradeoffs in Escherichia coli mutants adapted to prolonged starvation Journal Article
Journal of Genetics, 78 (1), pp. 43–49, 1999, ISSN: 0022-1333.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Vasi1999,
title = {Ecological strategies and fitness tradeoffs in \textit{Escherichia coli} mutants adapted to prolonged starvation},
author = {Farida K. Vasi and Richard E. Lenski},
url = {http://link.springer.com/10.1007/BF02994702},
doi = {10.1007/BF02994702},
issn = {0022-1333},
year = {1999},
date = {1999-04-01},
urldate = {1999-04-01},
journal = {Journal of Genetics},
volume = {78},
number = {1},
pages = {43--49},
abstract = {Many bacteria in nature are nutritionally deprived, and there has been heightened interest during the past decade in the properties of these bacteria. We subjected five populations of \textit{Escherichia coli} to prolonged starvation in a minimal salts medium, during which time the density of viable cells declined by several orders of magnitude. From each one, we isolated a surviving clone that showed some heritable difference in colony morphology. We then characterized these mutants in two ecologically relevant respects. First, we determined the nature of their selective advantage, if any, during prolonged starvation. (i) Three of the five mutants had significantly lower net death rate when progenitor and mutant clones were starved separately. (ii) Three mutants showed a significant reduction in death rate in mixed culture that was frequency dependent and manifest when the mutant clone was initially rare. This pattern suggests that these mutants fed on some byproduct of progenitor cells (living or dead). (iii) Two mutants caused the death rate of their progenitors to increase significantly relative to the rate measured in the absence of the mutant. This pattern suggests that these mutants had become allelopathic to their progenitors. Thus, three distinct ecological adaptations to prolonged starvation are evident. No advantage was detected for one mutant, whereas two mutants exhibited multiple advantages. Second, we asked whether the starvation-selected mutants were as fit in growth-supporting conditions as their progenitors. All five mutants were inferior to their progenitor during competition in fresh medium. Evidently, there is an evolutionary tradeoff between performance under growth and starvation conditions. },
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Many bacteria in nature are nutritionally deprived, and there has been heightened interest during the past decade in the properties of these bacteria. We subjected five populations of Escherichia coli to prolonged starvation in a minimal salts medium, during which time the density of viable cells declined by several orders of magnitude. From each one, we isolated a surviving clone that showed some heritable difference in colony morphology. We then characterized these mutants in two ecologically relevant respects. First, we determined the nature of their selective advantage, if any, during prolonged starvation. (i) Three of the five mutants had significantly lower net death rate when progenitor and mutant clones were starved separately. (ii) Three mutants showed a significant reduction in death rate in mixed culture that was frequency dependent and manifest when the mutant clone was initially rare. This pattern suggests that these mutants fed on some byproduct of progenitor cells (living or dead). (iii) Two mutants caused the death rate of their progenitors to increase significantly relative to the rate measured in the absence of the mutant. This pattern suggests that these mutants had become allelopathic to their progenitors. Thus, three distinct ecological adaptations to prolonged starvation are evident. No advantage was detected for one mutant, whereas two mutants exhibited multiple advantages. Second, we asked whether the starvation-selected mutants were as fit in growth-supporting conditions as their progenitors. All five mutants were inferior to their progenitor during competition in fresh medium. Evidently, there is an evolutionary tradeoff between performance under growth and starvation conditions.
de Visser J A G M; Zeyl C W; Gerrish P J; Blanchard J L; Lenski R E
Diminishing returns from mutation supply rate in asexual populations. Journal Article
Science, 283 , pp. 404-406, 1999, ISSN: 00368075.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments, Fitness Trajectories, Mutation Rates
@article{nokey,
title = {Diminishing returns from mutation supply rate in asexual populations.},
author = {J. Arjan G. M. {de Visser} and C. W. Zeyl and Philip J. Gerrish and Jeffrey L. Blanchard and Richard E. Lenski},
url = {https://www.science.org/lookup/doi/10.1126/science.283.5400.404},
doi = {10.1126/science.283.5400.404},
issn = {00368075},
year = {1999},
date = {1999-01-15},
urldate = {1999-01-15},
journal = {Science},
volume = {283},
pages = {404-406},
abstract = {Mutator genotypes with increased mutation rates may be especially important in microbial evolution if genetic adaptation is generally limited by the supply of mutations. In experimental populations of the bacterium \textit{Escherichia coli}, the rate of evolutionary adaptation was proportional to the mutation supply rate only in particular circumstances of small or initially well-adapted populations. These experiments also demonstrate a "speed limit" on adaptive evolution in asexual populations, one that is independent of the mutation supply rate.},
keywords = {Descendant Experiments, Fitness Trajectories, Mutation Rates},
pubstate = {published},
tppubtype = {article}
}
Mutator genotypes with increased mutation rates may be especially important in microbial evolution if genetic adaptation is generally limited by the supply of mutations. In experimental populations of the bacterium Escherichia coli, the rate of evolutionary adaptation was proportional to the mutation supply rate only in particular circumstances of small or initially well-adapted populations. These experiments also demonstrate a "speed limit" on adaptive evolution in asexual populations, one that is independent of the mutation supply rate.
1998
Turner P E; Cooper V S; Lenski R E
Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Journal Article
Evolution, 52 (2), pp. 315–329, 1998, ISSN: 0014-3820.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Turner1998,
title = {Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids.},
author = {Paul E. Turner and Vaughn S. Cooper and Richard E. Lenski},
url = {https://onlinelibrary.wiley.com/doi/10.1111/j.1558-5646.1998.tb01634.x},
doi = {10.1111/j.1558-5646.1998.tb01634.x},
issn = {0014-3820},
year = {1998},
date = {1998-04-01},
urldate = {1998-04-01},
journal = {Evolution},
volume = {52},
number = {2},
pages = {315--329},
abstract = {It has been hypothesized that there is a fundamental conflict between horizontal (infectious) and vertical (intergenerational) modes of parasite transmission. Activities of a parasite that increase its rate of infectious transmission are presumed to reduce its host's fitness. This reduction in host fitness impedes vertical transmission of the parasite and causes a tradeoff between horizontal and vertical transmission. Given this tradeoff, and assuming no multiple infections (no within-host competition among parasites), a simple model predicts that the density of uninfected hosts in the environment should determine the optimum balance between modes of parasite transmission. When susceptible hosts are abundant, selection should favor increased rates of horizontal transfer, even at the expense of reduced vertical transmission. Conversely, when hosts are rare, selection should favor increased vertical transmission even at the expense of lower horizontal transfer. We tested the tradeoff hypothesis and these evolutionary predictions using conjugative plasmids and the bacteria that they infect. Plasmids were allowed to evolve for 500 generations in environments with different densities of susceptible hosts. The plasmid's rate of horizontal transfer by conjugation increased at the expense of host fitness, indicating a tradeoff between horizontal and vertical transmission. Also, reductions in conjugation rate repeatedly coincided with the loss of a particular plasmid-encoded antibiotic resistance gene. However, susceptible host density had no significant effect on the evolution of horizontal versus vertical modes of plasmid transmission. We consider several possible explanations for the failure to observe such an effect.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
It has been hypothesized that there is a fundamental conflict between horizontal (infectious) and vertical (intergenerational) modes of parasite transmission. Activities of a parasite that increase its rate of infectious transmission are presumed to reduce its host's fitness. This reduction in host fitness impedes vertical transmission of the parasite and causes a tradeoff between horizontal and vertical transmission. Given this tradeoff, and assuming no multiple infections (no within-host competition among parasites), a simple model predicts that the density of uninfected hosts in the environment should determine the optimum balance between modes of parasite transmission. When susceptible hosts are abundant, selection should favor increased rates of horizontal transfer, even at the expense of reduced vertical transmission. Conversely, when hosts are rare, selection should favor increased vertical transmission even at the expense of lower horizontal transfer. We tested the tradeoff hypothesis and these evolutionary predictions using conjugative plasmids and the bacteria that they infect. Plasmids were allowed to evolve for 500 generations in environments with different densities of susceptible hosts. The plasmid's rate of horizontal transfer by conjugation increased at the expense of host fitness, indicating a tradeoff between horizontal and vertical transmission. Also, reductions in conjugation rate repeatedly coincided with the loss of a particular plasmid-encoded antibiotic resistance gene. However, susceptible host density had no significant effect on the evolution of horizontal versus vertical modes of plasmid transmission. We consider several possible explanations for the failure to observe such an effect.
Elena S F; Ekunwe L; Hajela N; Oden S A; Lenski R E
Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Journal Article
Genetica, 102-103 (1-6), pp. 349–58, 1998, ISSN: 0016-6707.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Elena1998,
title = {Distribution of fitness effects caused by random insertion mutations in \textit{Escherichia coli}.},
author = {Santiago F. Elena and Lynette Ekunwe and Neerja Hajela and Shenandoah A. Oden and Richard E. Lenski},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9720287},
doi = {10.1023/a:1017031008316},
issn = {0016-6707},
year = {1998},
date = {1998-01-01},
urldate = {1998-01-01},
journal = {Genetica},
volume = {102-103},
number = {1-6},
pages = {349--58},
abstract = {Very little is known about the distribution of mutational effects on organismal fitness, despite the fundamental importance of this information for the study of evolution. This lack of information reflects the fact that it is generally difficult to quantify the dynamic effects of mutation and natural selection using only static distributions of allele frequencies. In this study, we took a direct approach to measuring the effects of mutations on fitness. We used transposon-mutagenesis to create 226 mutant clones of \textit{Escherichia coli}. Each mutant clone carried a single random insertion of a derivative of Tn\textit{10}. All 226 mutants were independently derived from the same progenitor clone, which was obtained from a population that had evolved in a constant laboratory environment for 10,000 generations. We then performed competition experiments to measure the effect of each mutation on fitness relative to a common competitor. At least 80% of the mutations had a significant negative effect on fitness, whereas none of the mutations had a significant positive effect. The mutations reduced fitness by about 3%, on average, but the distribution of fitness effects was highly skewed and had a long, flat tail. A compound distribution, which includes both gamma and uniform components, provided an excellent fit to the observed fitness values.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Very little is known about the distribution of mutational effects on organismal fitness, despite the fundamental importance of this information for the study of evolution. This lack of information reflects the fact that it is generally difficult to quantify the dynamic effects of mutation and natural selection using only static distributions of allele frequencies. In this study, we took a direct approach to measuring the effects of mutations on fitness. We used transposon-mutagenesis to create 226 mutant clones of Escherichia coli. Each mutant clone carried a single random insertion of a derivative of Tn10. All 226 mutants were independently derived from the same progenitor clone, which was obtained from a population that had evolved in a constant laboratory environment for 10,000 generations. We then performed competition experiments to measure the effect of each mutation on fitness relative to a common competitor. At least 80% of the mutations had a significant negative effect on fitness, whereas none of the mutations had a significant positive effect. The mutations reduced fitness by about 3%, on average, but the distribution of fitness effects was highly skewed and had a long, flat tail. A compound distribution, which includes both gamma and uniform components, provided an excellent fit to the observed fitness values.
1997
Elena S F; Lenski R E
Test of synergistic interactions among deleterious mutations in bacteria Journal Article
Nature, 390 (6658), pp. 395–398, 1997, ISSN: 0028-0836.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Elena1997b,
title = {Test of synergistic interactions among deleterious mutations in bacteria},
author = {Santiago F. Elena and Richard E. Lenski},
url = {http://www.nature.com/articles/37108},
doi = {10.1038/37108},
issn = {0028-0836},
year = {1997},
date = {1997-11-01},
urldate = {1997-11-01},
journal = {Nature},
volume = {390},
number = {6658},
pages = {395--398},
abstract = {Identifying the forces responsible for the origin and maintenance of sexuality remains one of the greatest unsolved problems in biology. The mutational deterministic hypothesis postulates that sex is an adaptation that allows deleterious mutations to be purged from the genome; it requires synergistic interactions, which means that two mutations would be more harmful together than expected from their separate effects. We generated 225 genotypes of \textit{Escherichia coli} carrying one, two or three successive mutations and measured their fitness relative to an unmutated competitor. The relationship between mutation number and average fitness is nearly log- linear. We also constructed 27 recombinant genotypes having pairs of mutations whose separate and combined effects on fitness were determined. Several pairs exhibit significant interactions for fitness, but they are antagonistic as often as they are synergistic. These results do not support the mutational deterministic hypothesis for the evolution of sex.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Identifying the forces responsible for the origin and maintenance of sexuality remains one of the greatest unsolved problems in biology. The mutational deterministic hypothesis postulates that sex is an adaptation that allows deleterious mutations to be purged from the genome; it requires synergistic interactions, which means that two mutations would be more harmful together than expected from their separate effects. We generated 225 genotypes of Escherichia coli carrying one, two or three successive mutations and measured their fitness relative to an unmutated competitor. The relationship between mutation number and average fitness is nearly log- linear. We also constructed 27 recombinant genotypes having pairs of mutations whose separate and combined effects on fitness were determined. Several pairs exhibit significant interactions for fitness, but they are antagonistic as often as they are synergistic. These results do not support the mutational deterministic hypothesis for the evolution of sex.