2026
Donofrio M A; Blasius H L; Nguyen C C; Schnell A L; Turner C B
Antibiotic susceptibility of Escherichia coli is affected by evolutionary history but not by history of elemental limitation Journal Article
mSphere, vol. 11, iss. 4, pp. e00538-25, 2026.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Descendant Experiments, Genotypes and Phenotypes
@article{Donofrio2026,
title = {Antibiotic susceptibility of \textit{Escherichia coli} is affected by evolutionary history but not by history of elemental limitation},
author = {Marissa A. Donofrio and Heather L. Blasius and Catherine C. Nguyen and Alexa L. Schnell and Caroline B. Turner},
url = {https://journals.asm.org/doi/10.1128/msphere.00538-25},
doi = {10.1128/msphere.00538-25},
year = {2026},
date = {2026-03-23},
urldate = {2026-03-23},
journal = {mSphere},
volume = {11},
issue = {4},
pages = {e00538-25},
abstract = {ABSTRACT: Antibiotic resistance in bacteria is a global public health threat. To understand how the evolution of antibiotic susceptibility is affected by environmental conditions and prior evolutionary history, we worked with populations from the Long-Term Evolution Experiment (LTEE) with \textit{Escherichia coli}. These populations previously evolved independently for 50,000 generations in an environment without antibiotics, making them an ideal system for studying the effect of evolutionary history on adaptation to new selective pressures. We further evolved five of the LTEE populations, as well as their shared ancestor, under either carbon- or nitrogen-limited conditions and then tested intrinsic resistance to four antibiotics. Evolution under elemental limitation did not have a significant impact on resistance to any of the tested antibiotics. However, some LTEE populations did have higher resistance than other populations. Susceptibility also varied within one population, which had the lowest level of resistance to all four antibiotics. We hypothesized that resistance levels might differ between two clades of bacteria that have coexisted within this population for more than 40,000 generations. Interestingly, although antibiotic susceptibility varied within the population, there was no consistent difference between clades. Instead, one particular clone isolated from the population exhibited higher resistance than the other clones sampled. These findings indicate that antibiotic resistance can vary both within and between experimentally evolved populations, even in the absence of direct selection on resistance. Our results also show that measured levels of susceptibility may depend on stochastic sampling effects during isolation of clones. IMPORTANCE: Antibiotic resistance is one of the most pressing health challenges worldwide, and understanding how bacteria evolve resistance, even when not directly exposed to antibiotics, is critical for managing and predicting emerging threats. Our study leverages the unique Long-Term Evolution Experiment with \textit{Escherichia coli} to show that both the evolutionary history of bacterial populations and random variation among individual clones can significantly influence intrinsic antibiotic susceptibility. Our results also suggest that elemental limitation, while a critical environmental variable, may not be an important driver of intrinsic antibiotic susceptibility, at least over short time frames.},
keywords = {Correlated Responses, Descendant Experiments, Genotypes and Phenotypes},
pubstate = {published},
tppubtype = {article}
}
ABSTRACT: Antibiotic resistance in bacteria is a global public health threat. To understand how the evolution of antibiotic susceptibility is affected by environmental conditions and prior evolutionary history, we worked with populations from the Long-Term Evolution Experiment (LTEE) with Escherichia coli. These populations previously evolved independently for 50,000 generations in an environment without antibiotics, making them an ideal system for studying the effect of evolutionary history on adaptation to new selective pressures. We further evolved five of the LTEE populations, as well as their shared ancestor, under either carbon- or nitrogen-limited conditions and then tested intrinsic resistance to four antibiotics. Evolution under elemental limitation did not have a significant impact on resistance to any of the tested antibiotics. However, some LTEE populations did have higher resistance than other populations. Susceptibility also varied within one population, which had the lowest level of resistance to all four antibiotics. We hypothesized that resistance levels might differ between two clades of bacteria that have coexisted within this population for more than 40,000 generations. Interestingly, although antibiotic susceptibility varied within the population, there was no consistent difference between clades. Instead, one particular clone isolated from the population exhibited higher resistance than the other clones sampled. These findings indicate that antibiotic resistance can vary both within and between experimentally evolved populations, even in the absence of direct selection on resistance. Our results also show that measured levels of susceptibility may depend on stochastic sampling effects during isolation of clones. IMPORTANCE: Antibiotic resistance is one of the most pressing health challenges worldwide, and understanding how bacteria evolve resistance, even when not directly exposed to antibiotics, is critical for managing and predicting emerging threats. Our study leverages the unique Long-Term Evolution Experiment with Escherichia coli to show that both the evolutionary history of bacterial populations and random variation among individual clones can significantly influence intrinsic antibiotic susceptibility. Our results also suggest that elemental limitation, while a critical environmental variable, may not be an important driver of intrinsic antibiotic susceptibility, at least over short time frames.
2025
Chihoub D; Pintard C; Lenski R E; Tenaillon O; Couce A
The evolution of robustness and fragility during long-term bacterial adaptation Journal Article
Proceedings of the National Academy of Sciences of the United States of America, vol. 122, no. 16, pp. e2501901122, 2025.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Fitness Trajectories
@article{Chihoub2025,
title = {The evolution of robustness and fragility during long-term bacterial adaptation},
author = {Doha Chihoub and Coralie Pintard and Richard E. Lenski and Olivier Tenaillon and Alejandro Couce},
doi = {10.1073/pnas.2501901122},
year = {2025},
date = {2025-01-27},
urldate = {2025-01-27},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
volume = {122},
number = {16},
pages = {e2501901122},
abstract = {Theory predicts that well-adapted populations may evolve mechanisms to counteract the inevitable influx of deleterious mutations. While mutational robustness can be directly selected in the laboratory, evidence for its spontaneous evolution during general adaptation is mixed. Moreover, whether robustness evolves to include pleiotropic effects remains largely unexplored. Here, we studied the effects of point mutations in the RNA polymerase of \textit{Escherichia coli} over a 15,000-generation adaptive trajectory. Fitness effects of both beneficial and deleterious mutations were attenuated in fitter backgrounds. In contrast, pleiotropic effects became more severe and widespread with greater adaptation. These results show that trade-offs between robustness and fragility can evolve in regulatory networks, regardless of whether driven by adaptive or nonadaptive processes. More broadly, they illustrate how adaptation can generate hidden variability, with unpredictable evolutionary consequences in new environments.},
keywords = {Correlated Responses, Fitness Trajectories},
pubstate = {published},
tppubtype = {article}
}
Theory predicts that well-adapted populations may evolve mechanisms to counteract the inevitable influx of deleterious mutations. While mutational robustness can be directly selected in the laboratory, evidence for its spontaneous evolution during general adaptation is mixed. Moreover, whether robustness evolves to include pleiotropic effects remains largely unexplored. Here, we studied the effects of point mutations in the RNA polymerase of Escherichia coli over a 15,000-generation adaptive trajectory. Fitness effects of both beneficial and deleterious mutations were attenuated in fitter backgrounds. In contrast, pleiotropic effects became more severe and widespread with greater adaptation. These results show that trade-offs between robustness and fragility can evolve in regulatory networks, regardless of whether driven by adaptive or nonadaptive processes. More broadly, they illustrate how adaptation can generate hidden variability, with unpredictable evolutionary consequences in new environments.
2023
Jagdish T
The dynamics of fitness and pleiotropy in a long-term evolution experiment with Escherichia coli PhD Thesis
2023.
Abstract | Links | BibTeX | Tags: Correlated Responses, Demography and Ecology, Fitness Trajectories, Methods and Miscellaneous
@phdthesis{nokey,
title = {The dynamics of fitness and pleiotropy in a long-term evolution experiment with \textit{Escherichia coli}},
author = {Tanush Jagdish},
url = {https://dash.harvard.edu/handle/1/37375541},
year = {2023},
date = {2023-05-08},
urldate = {2023-05-08},
abstract = {Life on earth is shaped by a delicate balance between chance and necessity. A combination of natural selection and genetic drift has moulded random genetic variations over the course of billions of years to generate the complex and interconnected biosphere we see today. These evolutionary dynamics are ultimately the product of numerous genetic mechanisms operating in genomes with highly complex architectures. Unravelling the rules of genetic mechanisms responsible for evolutionary innovation is critical to developing a comprehensive and predictive evolutionary theory, but has evaded direct experimentation since the scale of resources and technology needed to study the patterns of genetic evolution has only recently become achievable. In this dissertation, I explore the use of microbial experimental evolution as a powerful tool for probing evolutionary questions, particularly by leveraging DNA-barcoding and high-throughput DNA sequencing. In chapter 1, I provide an overview of the field of microbial experimental evolution, dividing its history into two eras marked by qualitatively different methodological advancements. I make the case that we now stand at the dawn of a third era, where advances in genome-engineering coupled with low-cost, high-throughput DNA sequencing will allow experiments to finally probe evolution on a statistical scale. I then present two research studies that take advantage of microbial experimental evolution to investigate distinct genetic mechanisms key to the evolutionary process. In Chapter 2, I explore whether fitness can continue increasing in a population that has already adapted to its environment for over 30,000 generations, and whether fixations of beneficial mutations from population-wide DNA sequencing can predict jumps in fitness. My findings reveal that fitness continues to monotonically increase in step with the fixation of beneficial mutations, even though the rate of fixation has dramatically slowed down, highlighting the potential for ongoing adaptation even under constant environmental conditions. In Chapter 3, I develop a novel conjugation-based DNA-barcoding method for the Long-Term Evolution Experiment (LTEE) with \textit{Escherichia coli}, allowing me to examine the pleiotropic consequences of adaptation to glucose over 50,000 generations in 15 novel resource environments. My observations reveal broad patterns of both convergent and divergent evolution that correspond with mutations in key metabolic genes in clonal sequencing datasets, shedding light on the nature of pleiotropy and its evolution over extended timescales. Using microbial model systems in an evolutionary context has the unique advantage of being relevant both to fundamental evolutionary biology and human health. Since genetic drift and rare mutational events both play an outsized role in determining the evolutionary trajectories of populations, evolutionary questions in the modern age will increasingly be faced with issues of scale. Microbial experimental evolution offers both scale and tractability to solve this problem. Uniquely, this does not sacrifice on human relevance. Building a coarse-grained and comprehensive evolutionary theory is more significant to society today than ever before as the importance of clonal evolution in cancer, gut microbiomes and even pandemics becomes more clearly understood.},
keywords = {Correlated Responses, Demography and Ecology, Fitness Trajectories, Methods and Miscellaneous},
pubstate = {published},
tppubtype = {phdthesis}
}
Life on earth is shaped by a delicate balance between chance and necessity. A combination of natural selection and genetic drift has moulded random genetic variations over the course of billions of years to generate the complex and interconnected biosphere we see today. These evolutionary dynamics are ultimately the product of numerous genetic mechanisms operating in genomes with highly complex architectures. Unravelling the rules of genetic mechanisms responsible for evolutionary innovation is critical to developing a comprehensive and predictive evolutionary theory, but has evaded direct experimentation since the scale of resources and technology needed to study the patterns of genetic evolution has only recently become achievable. In this dissertation, I explore the use of microbial experimental evolution as a powerful tool for probing evolutionary questions, particularly by leveraging DNA-barcoding and high-throughput DNA sequencing. In chapter 1, I provide an overview of the field of microbial experimental evolution, dividing its history into two eras marked by qualitatively different methodological advancements. I make the case that we now stand at the dawn of a third era, where advances in genome-engineering coupled with low-cost, high-throughput DNA sequencing will allow experiments to finally probe evolution on a statistical scale. I then present two research studies that take advantage of microbial experimental evolution to investigate distinct genetic mechanisms key to the evolutionary process. In Chapter 2, I explore whether fitness can continue increasing in a population that has already adapted to its environment for over 30,000 generations, and whether fixations of beneficial mutations from population-wide DNA sequencing can predict jumps in fitness. My findings reveal that fitness continues to monotonically increase in step with the fixation of beneficial mutations, even though the rate of fixation has dramatically slowed down, highlighting the potential for ongoing adaptation even under constant environmental conditions. In Chapter 3, I develop a novel conjugation-based DNA-barcoding method for the Long-Term Evolution Experiment (LTEE) with Escherichia coli, allowing me to examine the pleiotropic consequences of adaptation to glucose over 50,000 generations in 15 novel resource environments. My observations reveal broad patterns of both convergent and divergent evolution that correspond with mutations in key metabolic genes in clonal sequencing datasets, shedding light on the nature of pleiotropy and its evolution over extended timescales. Using microbial model systems in an evolutionary context has the unique advantage of being relevant both to fundamental evolutionary biology and human health. Since genetic drift and rare mutational events both play an outsized role in determining the evolutionary trajectories of populations, evolutionary questions in the modern age will increasingly be faced with issues of scale. Microbial experimental evolution offers both scale and tractability to solve this problem. Uniquely, this does not sacrifice on human relevance. Building a coarse-grained and comprehensive evolutionary theory is more significant to society today than ever before as the importance of clonal evolution in cancer, gut microbiomes and even pandemics becomes more clearly understood.
2022
Mathé-Hubert H; Amie R; Martin M; Gaffé J; Schneider D
Evolution of bacterial persistence to antibiotics during a 50,000-generation experiment in an antibiotic-free environment Journal Article
Antibiotics, vol. 11, no. 4, pp. 451, 2022, ISSN: 2079-6382.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Genotypes and Phenotypes
@article{mathe-hubert2022,
title = {Evolution of bacterial persistence to antibiotics during a 50,000-generation experiment in an antibiotic-free environment},
author = {Hugo Mathé-Hubert and Rafika Amie and Mikaël Martin and Joël Gaffé and Dominique Schneider},
url = {https://www.mdpi.com/2079-6382/11/4/451},
doi = {10.3390/antibiotics11040451},
issn = {2079-6382},
year = {2022},
date = {2022-03-27},
urldate = {2022-03-27},
journal = {Antibiotics},
volume = {11},
number = {4},
pages = {451},
abstract = {Failure of antibiotic therapies causes >700,000 deaths yearly and involves both bacterial resistance and persistence. Persistence results in the relapse of infections by producing a tiny fraction of pathogen survivors that stay dormant during antibiotic exposure. From an evolutionary perspective, persistence is either a ‘bet-hedging strategy’ that helps to cope with stochastically changing environments or an unavoidable minimal rate of ‘cellular errors’ that lock the cells in a low activity state. Here, we analyzed the evolution of persistence over 50,000 bacterial generations in a stable environment by improving a published method that estimates the number of persister cells based on the growth of the reviving population. Our results challenged our understanding of the factors underlying persistence evolution. In one case, we observed a substantial decrease in persistence proportion, suggesting that the naturally observed persistence level is not an unavoidable minimal rate of ‘cellular errors’. However, although there was no obvious environmental stochasticity, in 11 of the 12 investigated populations, the persistence level was maintained during 50,000 bacterial generations.},
keywords = {Correlated Responses, Genotypes and Phenotypes},
pubstate = {published},
tppubtype = {article}
}
Failure of antibiotic therapies causes >700,000 deaths yearly and involves both bacterial resistance and persistence. Persistence results in the relapse of infections by producing a tiny fraction of pathogen survivors that stay dormant during antibiotic exposure. From an evolutionary perspective, persistence is either a ‘bet-hedging strategy’ that helps to cope with stochastically changing environments or an unavoidable minimal rate of ‘cellular errors’ that lock the cells in a low activity state. Here, we analyzed the evolution of persistence over 50,000 bacterial generations in a stable environment by improving a published method that estimates the number of persister cells based on the growth of the reviving population. Our results challenged our understanding of the factors underlying persistence evolution. In one case, we observed a substantial decrease in persistence proportion, suggesting that the naturally observed persistence level is not an unavoidable minimal rate of ‘cellular errors’. However, although there was no obvious environmental stochasticity, in 11 of the 12 investigated populations, the persistence level was maintained during 50,000 bacterial generations.
2021
van Raay K; Stolyar S; Sevigny J; Draghi J; Lenski R E; Marx C J; Kerr B; Zaman L
Evolution with private resources reverses some changes from long-term evolution with public resources Unpublished
bioRxiv, 2021.
Abstract | Links | BibTeX | Altmetric | Tags: Cell Morphology, Correlated Responses, Demography and Ecology, Descendant Experiments, Genotypes and Phenotypes, Historical Contingency, Methods and Miscellaneous
@unpublished{Raay2021,
title = {Evolution with private resources reverses some changes from long-term evolution with public resources},
author = {Katrina {van Raay} and Sergey Stolyar and Jordana Sevigny and Jeremy Draghi and Richard E. Lenski and Christopher J. Marx and Benjamin Kerr and Luis Zaman},
url = {https://www.biorxiv.org/content/10.1101/2021.07.11.451942v1},
doi = {https://doi.org/10.1101/2021.07.11.451942},
year = {2021},
date = {2021-07-12},
urldate = {2021-07-12},
journal = {bioRxiv},
pages = {2021.07.11.451942},
abstract = {A population under selection to improve one trait may evolve a sub-optimal state for another trait due to tradeoffs and other evolutionary constraints. How this evolution affects the capacity of a population to adapt when conditions change to favor the second trait is an open question. We investigated this question using isolates from a lineage spanning 60,000 generations of the Long-Term Evolution Experiment (LTEE) with \textit{Escherichia coli}, where cells have access to a shared pool of resources, and have evolved increased competitive ability and a concomitant reduction in numerical yield. Using media-in oil emulsions we shifted the focus of selection to numerical yield, where cells grew in isolated patches with private resources. We found that the time spent evolving under shared resources did not affect the ability to re-evolve toward higher numerical yield. The evolution of numerical yield commonly occurred through mutations in the phosphoenolpyruvate phosphotransferase system. These mutants exhibit slower uptake of glucose, making them poorer competitors for public resources, and produce smaller cells that release less carbon as overflow metabolites. Our results demonstrate that mutations that were not part of adaptation under one selective regime may enable access to ancestral phenotypes when selection changes to favor evolutionary reversion. },
howpublished = {bioRxiv},
keywords = {Cell Morphology, Correlated Responses, Demography and Ecology, Descendant Experiments, Genotypes and Phenotypes, Historical Contingency, Methods and Miscellaneous},
pubstate = {published},
tppubtype = {unpublished}
}
A population under selection to improve one trait may evolve a sub-optimal state for another trait due to tradeoffs and other evolutionary constraints. How this evolution affects the capacity of a population to adapt when conditions change to favor the second trait is an open question. We investigated this question using isolates from a lineage spanning 60,000 generations of the Long-Term Evolution Experiment (LTEE) with Escherichia coli, where cells have access to a shared pool of resources, and have evolved increased competitive ability and a concomitant reduction in numerical yield. Using media-in oil emulsions we shifted the focus of selection to numerical yield, where cells grew in isolated patches with private resources. We found that the time spent evolving under shared resources did not affect the ability to re-evolve toward higher numerical yield. The evolution of numerical yield commonly occurred through mutations in the phosphoenolpyruvate phosphotransferase system. These mutants exhibit slower uptake of glucose, making them poorer competitors for public resources, and produce smaller cells that release less carbon as overflow metabolites. Our results demonstrate that mutations that were not part of adaptation under one selective regime may enable access to ancestral phenotypes when selection changes to favor evolutionary reversion.
Grant N A; Maddamsetti R; Lenski R E
Maintenance of Metabolic Plasticity despite Relaxed Selection in a Long-Term Evolution Experiment with Escherichia coli Journal Article
The American Naturalist, vol. 198, no. 1, pp. 93–112, 2021, ISSN: 0003-0147.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Fitness Trajectories, Genome Evolution, Genotypes and Phenotypes
@article{Grant2021b,
title = {Maintenance of Metabolic Plasticity despite Relaxed Selection in a Long-Term Evolution Experiment with \textit{Escherichia coli}},
author = {Nkrumah A. Grant and Rohan Maddamsetti and Richard E. Lenski},
url = {https://www.journals.uchicago.edu/doi/10.1086/714530},
doi = {10.1086/714530},
issn = {0003-0147},
year = {2021},
date = {2021-07-01},
urldate = {2021-07-01},
journal = {The American Naturalist},
volume = {198},
number = {1},
pages = {93--112},
abstract = {Traits that are unused in a given environment are subject to processes that tend to erode them, leading to reduced fitness in other environments. Although this general tendency is clear, we know much less about why some traits are lost while others are retained and about the roles of mutation and selection in generating different responses. We addressed these issues by examining populations of a facultative anaerobe, \textit{Escherichia coli}, that have evolved for 130 years in the presence of oxygen, with relaxed selection for anaerobic growth and the associated metabolic plasticity. We asked whether evolution led to the loss, improvement, or maintenance of anaerobic growth, and we analyzed gene expression and mutational data sets to understand the outcomes. We identified genomic signatures of both positive and purifying selection on aerobic-specific genes, while anaerobic-specific genes showed clear evidence of relaxed selection. We also found parallel evolution at two interacting loci that regulate anaerobic growth. We competed the ancestor and evolved clones from each population in an anoxic environment, and we found that anaerobic fitness had not decayed, despite relaxed selection. In summary, relaxed selection does not necessarily reduce an organism's fitness in other environments. Instead, the genetic architecture of the traits under relaxed selection and their correlations with traits under positive and purifying selection may sometimes determine evolutionary outcomes.},
keywords = {Correlated Responses, Fitness Trajectories, Genome Evolution, Genotypes and Phenotypes},
pubstate = {published},
tppubtype = {article}
}
Traits that are unused in a given environment are subject to processes that tend to erode them, leading to reduced fitness in other environments. Although this general tendency is clear, we know much less about why some traits are lost while others are retained and about the roles of mutation and selection in generating different responses. We addressed these issues by examining populations of a facultative anaerobe, Escherichia coli, that have evolved for 130 years in the presence of oxygen, with relaxed selection for anaerobic growth and the associated metabolic plasticity. We asked whether evolution led to the loss, improvement, or maintenance of anaerobic growth, and we analyzed gene expression and mutational data sets to understand the outcomes. We identified genomic signatures of both positive and purifying selection on aerobic-specific genes, while anaerobic-specific genes showed clear evidence of relaxed selection. We also found parallel evolution at two interacting loci that regulate anaerobic growth. We competed the ancestor and evolved clones from each population in an anoxic environment, and we found that anaerobic fitness had not decayed, despite relaxed selection. In summary, relaxed selection does not necessarily reduce an organism's fitness in other environments. Instead, the genetic architecture of the traits under relaxed selection and their correlations with traits under positive and purifying selection may sometimes determine evolutionary outcomes.
2019
Card K J; LaBar T; Gomez J B; Lenski R E
Historical contingency in the evolution of antibiotic resistance after decades of relaxed selection Journal Article
PLOS Biology, vol. 17, no. 10, pp. e3000397, 2019, ISSN: 1545-7885.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Descendant Experiments, Historical Contingency
@article{nokey,
title = {Historical contingency in the evolution of antibiotic resistance after decades of relaxed selection},
author = {Kyle J. Card and Thomas LaBar and Jasper B. Gomez and Richard E. Lenski},
url = {https://dx.plos.org/10.1371/journal.pbio.3000397},
doi = {10.1371/journal.pbio.3000397},
issn = {1545-7885},
year = {2019},
date = {2019-10-23},
urldate = {2019-10-23},
journal = {PLOS Biology},
volume = {17},
number = {10},
pages = {e3000397},
abstract = {Populations often encounter changed environments that remove selection for the maintenance of particular phenotypic traits. The resulting genetic decay of those traits under relaxed selection reduces an organism’s fitness in its prior environment. However, whether and how such decay alters the subsequent evolvability of a population upon restoration of selection for a previously diminished trait is not well understood. We addressed this question using \textit{Escherichia coli} strains from the long-term evolution experiment (LTEE) that independently evolved for multiple decades in the absence of antibiotics. We first confirmed that these derived strains are typically more sensitive to various antibiotics than their common ancestor. We then subjected the ancestral and derived strains to various concentrations of these drugs to examine their potential to evolve increased resistance. We found that evolvability was idiosyncratic with respect to initial genotype; that is, the derived strains did not generally compensate for their greater susceptibility by “catching up” to the resistance level of the ancestor. Instead, the capacity to evolve increased resistance was constrained in some backgrounds, implying that evolvability depended upon prior mutations in a historically contingent fashion. We further subjected a time series of clones from one LTEE population to tetracycline and determined that an evolutionary constraint arose early in that population, corroborating the role of contingency. In summary, relaxed selection not only can drive populations to increased antibiotic susceptibility, but it can also affect the subsequent evolvability of antibiotic resistance in an unpredictable manner. This conclusion has potential implications for public health, and it underscores the need to consider the genetic context of pathogens when designing drug-treatment strategies.},
keywords = {Correlated Responses, Descendant Experiments, Historical Contingency},
pubstate = {published},
tppubtype = {article}
}
Populations often encounter changed environments that remove selection for the maintenance of particular phenotypic traits. The resulting genetic decay of those traits under relaxed selection reduces an organism’s fitness in its prior environment. However, whether and how such decay alters the subsequent evolvability of a population upon restoration of selection for a previously diminished trait is not well understood. We addressed this question using Escherichia coli strains from the long-term evolution experiment (LTEE) that independently evolved for multiple decades in the absence of antibiotics. We first confirmed that these derived strains are typically more sensitive to various antibiotics than their common ancestor. We then subjected the ancestral and derived strains to various concentrations of these drugs to examine their potential to evolve increased resistance. We found that evolvability was idiosyncratic with respect to initial genotype; that is, the derived strains did not generally compensate for their greater susceptibility by “catching up” to the resistance level of the ancestor. Instead, the capacity to evolve increased resistance was constrained in some backgrounds, implying that evolvability depended upon prior mutations in a historically contingent fashion. We further subjected a time series of clones from one LTEE population to tetracycline and determined that an evolutionary constraint arose early in that population, corroborating the role of contingency. In summary, relaxed selection not only can drive populations to increased antibiotic susceptibility, but it can also affect the subsequent evolvability of antibiotic resistance in an unpredictable manner. This conclusion has potential implications for public health, and it underscores the need to consider the genetic context of pathogens when designing drug-treatment strategies.
Lamrabet O; Martin M; Lenski R E; Schneider D
Changes in Intrinsic Antibiotic Susceptibility during a Long-Term Evolution Experiment with Escherichia coli Journal Article
mBio, vol. 10, no. 2, pp. 1–12, 2019, ISSN: 2161-2129.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses
@article{Lamrabet2019,
title = {Changes in Intrinsic Antibiotic Susceptibility during a Long-Term Evolution Experiment with \textit{Escherichia coli}},
author = {Otmane Lamrabet and Mikaël Martin and Richard E. Lenski and Dominique Schneider},
editor = {Julian E. Davies},
url = {https://journals.asm.org/doi/10.1128/mBio.00189-19},
doi = {10.1128/mBio.00189-19},
issn = {2161-2129},
year = {2019},
date = {2019-04-01},
urldate = {2019-04-01},
journal = {mBio},
volume = {10},
number = {2},
pages = {1--12},
abstract = {Resistance to antibiotics often evolves when bacteria encounter antibiotics. However, bacterial strains and species without any known exposure to these drugs also vary in their intrinsic susceptibility. In many cases, evolved resistance has been shown to be costly to the bacteria, such that resistant types have reduced competitiveness relative to their sensitive progenitors in the absence of antibiotics. In this study, we examined changes in the susceptibilities of 12 populations of \textit{Escherichia coli} to 15 antibiotics after 2,000 and 50,000 generations without exposure to any drug. The evolved bacteria tended to become more susceptible to most antibiotics, with most of the change occurring during the first 2,000 generations, when the bacteria were undergoing rapid adaptation to their experimental conditions. On balance, our findings indicate that bacteria with low levels of intrinsic resistance can, in the absence of relevant selection, become even more susceptible to antibiotics.},
keywords = {Correlated Responses},
pubstate = {published},
tppubtype = {article}
}
Resistance to antibiotics often evolves when bacteria encounter antibiotics. However, bacterial strains and species without any known exposure to these drugs also vary in their intrinsic susceptibility. In many cases, evolved resistance has been shown to be costly to the bacteria, such that resistant types have reduced competitiveness relative to their sensitive progenitors in the absence of antibiotics. In this study, we examined changes in the susceptibilities of 12 populations of Escherichia coli to 15 antibiotics after 2,000 and 50,000 generations without exposure to any drug. The evolved bacteria tended to become more susceptible to most antibiotics, with most of the change occurring during the first 2,000 generations, when the bacteria were undergoing rapid adaptation to their experimental conditions. On balance, our findings indicate that bacteria with low levels of intrinsic resistance can, in the absence of relevant selection, become even more susceptible to antibiotics.
2014
Leiby N; Marx C J
PLoS Biology, vol. 12, no. 2, pp. e1001789, 2014, ISSN: 1545-7885.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Mutation Rates
@article{Leiby2014,
title = {Metabolic Erosion Primarily Through Mutation Accumulation, and Not Tradeoffs, Drives Limited Evolution of Substrate Specificity in \textit{Escherichia coli}},
author = {Nicholas Leiby and Christopher J. Marx},
editor = {Nancy A. Moran},
url = {https://dx.plos.org/10.1371/journal.pbio.1001789},
doi = {10.1371/journal.pbio.1001789},
issn = {1545-7885},
year = {2014},
date = {2014-02-01},
urldate = {2014-02-01},
journal = {PLoS Biology},
volume = {12},
number = {2},
pages = {e1001789},
abstract = {Evolutionary adaptation to a constant environment is often accompanied by specialization and a reduction of fitness in other environments. We assayed the ability of the Lenski \textit{Escherichia coli} populations to grow on a range of carbon sources after 50,000 generations of adaptation on glucose. Using direct measurements of growth rates, we demonstrated that declines in performance were much less widespread than suggested by previous results from Biolog assays of cellular respiration. Surprisingly, there were many performance increases on a variety of substrates. In addition to the now famous example of citrate, we observed several other novel gains of function for organic acids that the ancestral strain only marginally utilized. Quantitative growth data also showed that strains with a higher mutation rate exhibited significantly more declines, suggesting that most metabolic erosion was driven by mutation accumulation and not by physiological tradeoffs. These reductions in growth by mutator strains were ameliorated by growth at lower temperature, consistent with the hypothesis that this metabolic erosion is largely caused by destabilizing mutations to the associated enzymes. We further hypothesized that reductions in growth rate would be greatest for substrates used most differently from glucose, and we used flux balance analysis to formulate this question quantitatively. To our surprise, we found no significant relationship between decreases in growth and dissimilarity to glucose metabolism. Taken as a whole, these data suggest that in a single resource environment, specialization does not mainly result as an inevitable consequence of adaptive tradeoffs, but rather due to the gradual accumulation of disabling mutations in unused portions of the genome. },
keywords = {Correlated Responses, Mutation Rates},
pubstate = {published},
tppubtype = {article}
}
Evolutionary adaptation to a constant environment is often accompanied by specialization and a reduction of fitness in other environments. We assayed the ability of the Lenski Escherichia coli populations to grow on a range of carbon sources after 50,000 generations of adaptation on glucose. Using direct measurements of growth rates, we demonstrated that declines in performance were much less widespread than suggested by previous results from Biolog assays of cellular respiration. Surprisingly, there were many performance increases on a variety of substrates. In addition to the now famous example of citrate, we observed several other novel gains of function for organic acids that the ancestral strain only marginally utilized. Quantitative growth data also showed that strains with a higher mutation rate exhibited significantly more declines, suggesting that most metabolic erosion was driven by mutation accumulation and not by physiological tradeoffs. These reductions in growth by mutator strains were ameliorated by growth at lower temperature, consistent with the hypothesis that this metabolic erosion is largely caused by destabilizing mutations to the associated enzymes. We further hypothesized that reductions in growth rate would be greatest for substrates used most differently from glucose, and we used flux balance analysis to formulate this question quantitatively. To our surprise, we found no significant relationship between decreases in growth and dissimilarity to glucose metabolism. Taken as a whole, these data suggest that in a single resource environment, specialization does not mainly result as an inevitable consequence of adaptive tradeoffs, but rather due to the gradual accumulation of disabling mutations in unused portions of the genome.
2012
Leiby N; Harcombe W R; Marx C J
BMC Evolutionary Biology, vol. 12, no. 1, pp. 151, 2012, ISSN: 1471-2148.
Abstract | Links | BibTeX | Altmetric | Tags: Citrate Evolution, Correlated Responses
@article{Leiby2012,
title = {Multiple long-term, experimentally-evolved populations of \textit{Escherichia coli} acquire dependence upon citrate as an iron chelator for optimal growth on glucose},
author = {Nicholas Leiby and William R. Harcombe and Christopher J. Marx},
url = {https://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-12-151},
doi = {10.1186/1471-2148-12-151},
issn = {1471-2148},
year = {2012},
date = {2012-12-01},
urldate = {2012-12-01},
journal = {BMC Evolutionary Biology},
volume = {12},
number = {1},
pages = {151},
abstract = {Background
Specialization for ecological niches is a balance of evolutionary adaptation and its accompanying tradeoffs. Here we focus on the Lenski Long-Term Evolution Experiment, which has maintained cultures of \textit{Escherichia coli} in the same defined seasonal environment for 50,000 generations. Over this time, much adaptation and specialization to the environment has occurred. The presence of citrate in the growth media selected one lineage to gain the novel ability to utilize citrate as a carbon source after 31,000 generations. Here we test whether other strains have specialized to rely on citrate after 50,000 generations.
Results
We show that in addition to the citrate-catabolizing strain, three other lineages evolving in parallel have acquired a dependence on citrate for optimal growth on glucose. None of these strains were stimulated indirectly by the sodium present in disodium citrate, nor exhibited even partial utilization of citrate as a carbon source. Instead, all three of these citrate-stimulated populations appear to rely on it as a chelator of iron.
Conclusions
The strains we examine here have evolved specialization to their environment through apparent loss of function. Our results are most consistent with the accumulation of mutations in iron transport genes that were obviated by abundant citrate. The results present another example where a subtle decision in the design of an evolution experiment led to unexpected evolutionary outcomes.},
keywords = {Citrate Evolution, Correlated Responses},
pubstate = {published},
tppubtype = {article}
}
Background
Specialization for ecological niches is a balance of evolutionary adaptation and its accompanying tradeoffs. Here we focus on the Lenski Long-Term Evolution Experiment, which has maintained cultures of Escherichia coli in the same defined seasonal environment for 50,000 generations. Over this time, much adaptation and specialization to the environment has occurred. The presence of citrate in the growth media selected one lineage to gain the novel ability to utilize citrate as a carbon source after 31,000 generations. Here we test whether other strains have specialized to rely on citrate after 50,000 generations.
Results
We show that in addition to the citrate-catabolizing strain, three other lineages evolving in parallel have acquired a dependence on citrate for optimal growth on glucose. None of these strains were stimulated indirectly by the sodium present in disodium citrate, nor exhibited even partial utilization of citrate as a carbon source. Instead, all three of these citrate-stimulated populations appear to rely on it as a chelator of iron.
Conclusions
The strains we examine here have evolved specialization to their environment through apparent loss of function. Our results are most consistent with the accumulation of mutations in iron transport genes that were obviated by abundant citrate. The results present another example where a subtle decision in the design of an evolution experiment led to unexpected evolutionary outcomes.
Specialization for ecological niches is a balance of evolutionary adaptation and its accompanying tradeoffs. Here we focus on the Lenski Long-Term Evolution Experiment, which has maintained cultures of Escherichia coli in the same defined seasonal environment for 50,000 generations. Over this time, much adaptation and specialization to the environment has occurred. The presence of citrate in the growth media selected one lineage to gain the novel ability to utilize citrate as a carbon source after 31,000 generations. Here we test whether other strains have specialized to rely on citrate after 50,000 generations.
Results
We show that in addition to the citrate-catabolizing strain, three other lineages evolving in parallel have acquired a dependence on citrate for optimal growth on glucose. None of these strains were stimulated indirectly by the sodium present in disodium citrate, nor exhibited even partial utilization of citrate as a carbon source. Instead, all three of these citrate-stimulated populations appear to rely on it as a chelator of iron.
Conclusions
The strains we examine here have evolved specialization to their environment through apparent loss of function. Our results are most consistent with the accumulation of mutations in iron transport genes that were obviated by abundant citrate. The results present another example where a subtle decision in the design of an evolution experiment led to unexpected evolutionary outcomes.
2010
Meyer J R; Agrawal A A; Quick R T; Dobias D T; Schneider D; Lenski R E
Parallel changes in host resistance to viral infection during 45,000 generations of relaxed selection Journal Article
Evolution, vol. 64, no. 10, pp. no–no, 2010, ISSN: 00143820.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Genotypes and Phenotypes, Parallelism and Divergence
@article{Meyer2010,
title = {Parallel changes in host resistance to viral infection during 45,000 generations of relaxed selection},
author = {Justin R. Meyer and Anurag A. Agrawal and Ryan T. Quick and Devin T. Dobias and Dominique Schneider and Richard E. Lenski},
url = {https://onlinelibrary.wiley.com/doi/10.1111/j.1558-5646.2010.01049.x},
doi = {10.1111/j.1558-5646.2010.01049.x},
issn = {00143820},
year = {2010},
date = {2010-08-01},
urldate = {2010-08-01},
journal = {Evolution},
volume = {64},
number = {10},
pages = {no--no},
abstract = {The dynamics of host susceptibility to parasites are often influenced by trade-offs between the costs and benefits of resistance. We assayed changes in the resistance to three viruses in six lines of \textit{Escherichia coli} that had been evolving for almost 45,000 generations in their absence. The common ancestor of these lines was completely resistant to T6, partially resistant to T6* (a mutant of T6 with altered host range), and sensitive to lambda. None of the populations changed with respect to resistance to T6, whereas all six evolved increased susceptibility to T6*, probably ameliorating a cost of resistance. More surprisingly, however, the majority of lines evolved complete resistance to lambda, despite not encountering that virus during this period. By coupling our results with previous work, we infer that resistance to lambda evolved as a pleiotropic effect of a beneficial mutation that downregulated an unused metabolic pathway. The strong parallelism between the lines implies that selection had almost deterministic effects on the evolution of these patterns of host resistance. The opposite outcomes for resistance to T6* and lambda demonstrate that the evolution of host resistance under relaxed selection cannot be fully predicted by simple trade-off models.},
keywords = {Correlated Responses, Genotypes and Phenotypes, Parallelism and Divergence},
pubstate = {published},
tppubtype = {article}
}
The dynamics of host susceptibility to parasites are often influenced by trade-offs between the costs and benefits of resistance. We assayed changes in the resistance to three viruses in six lines of Escherichia coli that had been evolving for almost 45,000 generations in their absence. The common ancestor of these lines was completely resistant to T6, partially resistant to T6* (a mutant of T6 with altered host range), and sensitive to lambda. None of the populations changed with respect to resistance to T6, whereas all six evolved increased susceptibility to T6*, probably ameliorating a cost of resistance. More surprisingly, however, the majority of lines evolved complete resistance to lambda, despite not encountering that virus during this period. By coupling our results with previous work, we infer that resistance to lambda evolved as a pleiotropic effect of a beneficial mutation that downregulated an unused metabolic pathway. The strong parallelism between the lines implies that selection had almost deterministic effects on the evolution of these patterns of host resistance. The opposite outcomes for resistance to T6* and lambda demonstrate that the evolution of host resistance under relaxed selection cannot be fully predicted by simple trade-off models.
2006
Sleight S C; Wigginton N S; Lenski R E
Increased susceptibility to repeated freeze-thaw cycles in Escherichia coli following long-term evolution in a benign environment. Journal Article
BMC evolutionary biology, vol. 6, no. February, pp. 104, 2006, ISSN: 1471-2148.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses
@article{Sleight2006,
title = {Increased susceptibility to repeated freeze-thaw cycles in \textit{Escherichia coli} following long-term evolution in a benign environment.},
author = {Sean C. Sleight and Nicholas S. Wigginton and Richard E. Lenski},
url = {http://www.ncbi.nlm.nih.gov/pubmed/17147797
http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC1698501},
doi = {10.1186/1471-2148-6-104},
issn = {1471-2148},
year = {2006},
date = {2006-12-01},
urldate = {2006-12-01},
journal = {BMC evolutionary biology},
volume = {6},
number = {February},
pages = {104},
abstract = {Background
In order to study the dynamics of evolutionary change, 12 populations of \textit{E. coli} B were serially propagated for 20,000 generations in minimal glucose medium at constant 37 degrees C. Correlated changes in various other traits have been previously associated with the improvement in competitive fitness in the selective environment. This study examines whether these evolved lines changed in their ability to tolerate the stresses of prolonged freezing and repeated freeze-thaw cycles during adaptation to a benign environment.
Results
All 12 lines that evolved in the benign environment for 20,000 generations are more sensitive to freeze-thaw cycles than their ancestor. The evolved lines have an average mortality rate of 54% per daily cycle, compared to the ancestral rate of 34%. By contrast, there was no significant difference between the evolved lines and their ancestor in mortality during prolonged freezing. There was also some variability among the evolved lines in susceptibility to repeated freeze-thaw cycles. Those lines that had evolved higher competitive fitness in the minimal glucose medium at 37 degrees C also had higher mortality during freeze-thaw cycles. This variability was not associated, however, with differences among lines in DNA repair functionality and mutability.
Conclusion
The consistency of the evolutionary declines in freeze-thaw tolerance, the correlation between fitness in glucose medium at 37 degrees C and mortality during freeze-thaw cycles, and the absence of greater declines in freeze-thaw survival among the hypermutable lines all indicate a trade-off between performance in minimal glucose medium at 37 degrees C and the capacity to tolerate this stress. Analyses of the mutations that enhance fitness at 37 degrees C may shed light on the physiological basis of this trade-off.},
keywords = {Correlated Responses},
pubstate = {published},
tppubtype = {article}
}
Background
In order to study the dynamics of evolutionary change, 12 populations of E. coli B were serially propagated for 20,000 generations in minimal glucose medium at constant 37 degrees C. Correlated changes in various other traits have been previously associated with the improvement in competitive fitness in the selective environment. This study examines whether these evolved lines changed in their ability to tolerate the stresses of prolonged freezing and repeated freeze-thaw cycles during adaptation to a benign environment.
Results
All 12 lines that evolved in the benign environment for 20,000 generations are more sensitive to freeze-thaw cycles than their ancestor. The evolved lines have an average mortality rate of 54% per daily cycle, compared to the ancestral rate of 34%. By contrast, there was no significant difference between the evolved lines and their ancestor in mortality during prolonged freezing. There was also some variability among the evolved lines in susceptibility to repeated freeze-thaw cycles. Those lines that had evolved higher competitive fitness in the minimal glucose medium at 37 degrees C also had higher mortality during freeze-thaw cycles. This variability was not associated, however, with differences among lines in DNA repair functionality and mutability.
Conclusion
The consistency of the evolutionary declines in freeze-thaw tolerance, the correlation between fitness in glucose medium at 37 degrees C and mortality during freeze-thaw cycles, and the absence of greater declines in freeze-thaw survival among the hypermutable lines all indicate a trade-off between performance in minimal glucose medium at 37 degrees C and the capacity to tolerate this stress. Analyses of the mutations that enhance fitness at 37 degrees C may shed light on the physiological basis of this trade-off.
In order to study the dynamics of evolutionary change, 12 populations of E. coli B were serially propagated for 20,000 generations in minimal glucose medium at constant 37 degrees C. Correlated changes in various other traits have been previously associated with the improvement in competitive fitness in the selective environment. This study examines whether these evolved lines changed in their ability to tolerate the stresses of prolonged freezing and repeated freeze-thaw cycles during adaptation to a benign environment.
Results
All 12 lines that evolved in the benign environment for 20,000 generations are more sensitive to freeze-thaw cycles than their ancestor. The evolved lines have an average mortality rate of 54% per daily cycle, compared to the ancestral rate of 34%. By contrast, there was no significant difference between the evolved lines and their ancestor in mortality during prolonged freezing. There was also some variability among the evolved lines in susceptibility to repeated freeze-thaw cycles. Those lines that had evolved higher competitive fitness in the minimal glucose medium at 37 degrees C also had higher mortality during freeze-thaw cycles. This variability was not associated, however, with differences among lines in DNA repair functionality and mutability.
Conclusion
The consistency of the evolutionary declines in freeze-thaw tolerance, the correlation between fitness in glucose medium at 37 degrees C and mortality during freeze-thaw cycles, and the absence of greater declines in freeze-thaw survival among the hypermutable lines all indicate a trade-off between performance in minimal glucose medium at 37 degrees C and the capacity to tolerate this stress. Analyses of the mutations that enhance fitness at 37 degrees C may shed light on the physiological basis of this trade-off.
2005
Ostrowski E A; Rozen D E; Lenski R E
Pleiotropic effects of beneficial mutations in Escherichia coli Journal Article
Evolution, vol. 59, no. 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.
2002
Cooper V S
Long-term experimental evolution in Escherichia coli. X. Quantifying the fundamental and realized niche. Journal Article
BMC Evolutionary Biology, vol. 9, pp. 1–9, 2002.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses
@article{Cooper2002,
title = {Long-term experimental evolution in \textit{Escherichia coli}. X. Quantifying the fundamental and realized niche.},
author = {Vaughn S. Cooper},
url = {https://bmcecolevol.biomedcentral.com/articles/10.1186/1471-2148-2-12},
doi = {https://doi.org/10.1186/1471-2148-2-12},
year = {2002},
date = {2002-01-01},
urldate = {2002-01-01},
journal = {BMC Evolutionary Biology},
volume = {9},
pages = {1--9},
abstract = {Background
Twelve populations of the bacterium, \textit{Escherichia coli}, adapted to a simple, glucose-limited, laboratory environment over 10,000 generations. As a consequence, these populations tended to lose functionality on alternative resources. I examined whether these populations in turn became inferior competitors in four alternative environments. These experiments are among the first to quantify and compare dimensions of the fundamental and realized niches.
Results
Three clones were isolated from each of the twelve populations after 10,000 generations of evolution. Direct competition between these clones and the ancestor in the selective environment revealed average fitness improvements of ~50%. When grown in the wells of Biolog plates, however, evolved clones grew 25% worse on average than the ancestor on a variety of different carbon sources. Next, I competed each evolved population versus the ancestor in four foreign environments (10-fold higher and lower glucose concentration, added bile salts, and dilute LB media). Surprisingly, nearly all populations were more fit than the ancestor in each foreign environment, though the margin of improvement was least in the most different environment. Most populations also evolved increased sensitivity to novobiocin.
Conclusions
Reduced functionality on numerous carbon sources suggested that the fundamental niche of twelve \textit{E. coli} populations had narrowed after adapting to a specific laboratory environment. However, in spite of these results, the same populations were competitively superior in four novel environments. These findings suggest that adaptation to certain dimensions of the environment may compensate for other functional losses and apparently enhance the realized niche.},
keywords = {Correlated Responses},
pubstate = {published},
tppubtype = {article}
}
Background
Twelve populations of the bacterium, Escherichia coli, adapted to a simple, glucose-limited, laboratory environment over 10,000 generations. As a consequence, these populations tended to lose functionality on alternative resources. I examined whether these populations in turn became inferior competitors in four alternative environments. These experiments are among the first to quantify and compare dimensions of the fundamental and realized niches.
Results
Three clones were isolated from each of the twelve populations after 10,000 generations of evolution. Direct competition between these clones and the ancestor in the selective environment revealed average fitness improvements of ~50%. When grown in the wells of Biolog plates, however, evolved clones grew 25% worse on average than the ancestor on a variety of different carbon sources. Next, I competed each evolved population versus the ancestor in four foreign environments (10-fold higher and lower glucose concentration, added bile salts, and dilute LB media). Surprisingly, nearly all populations were more fit than the ancestor in each foreign environment, though the margin of improvement was least in the most different environment. Most populations also evolved increased sensitivity to novobiocin.
Conclusions
Reduced functionality on numerous carbon sources suggested that the fundamental niche of twelve E. coli populations had narrowed after adapting to a specific laboratory environment. However, in spite of these results, the same populations were competitively superior in four novel environments. These findings suggest that adaptation to certain dimensions of the environment may compensate for other functional losses and apparently enhance the realized niche.
Twelve populations of the bacterium, Escherichia coli, adapted to a simple, glucose-limited, laboratory environment over 10,000 generations. As a consequence, these populations tended to lose functionality on alternative resources. I examined whether these populations in turn became inferior competitors in four alternative environments. These experiments are among the first to quantify and compare dimensions of the fundamental and realized niches.
Results
Three clones were isolated from each of the twelve populations after 10,000 generations of evolution. Direct competition between these clones and the ancestor in the selective environment revealed average fitness improvements of ~50%. When grown in the wells of Biolog plates, however, evolved clones grew 25% worse on average than the ancestor on a variety of different carbon sources. Next, I competed each evolved population versus the ancestor in four foreign environments (10-fold higher and lower glucose concentration, added bile salts, and dilute LB media). Surprisingly, nearly all populations were more fit than the ancestor in each foreign environment, though the margin of improvement was least in the most different environment. Most populations also evolved increased sensitivity to novobiocin.
Conclusions
Reduced functionality on numerous carbon sources suggested that the fundamental niche of twelve E. coli populations had narrowed after adapting to a specific laboratory environment. However, in spite of these results, the same populations were competitively superior in four novel environments. These findings suggest that adaptation to certain dimensions of the environment may compensate for other functional losses and apparently enhance the realized niche.
2001
Cooper V S; Schneider D; Blot M; Lenski R E
Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B Journal Article
Journal of Bacteriology, vol. 183, no. 9, pp. 2834-2841, 2001, ISSN: 0021-9193.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Genotypes and Phenotypes
@article{nokey,
title = {Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of \textit{Escherichia coli} B},
author = {Vaughn S. Cooper and Dominique Schneider and Michel Blot and Richard E. Lenski},
url = {https://journals.asm.org/doi/full/10.1128/JB.183.9.2834-2841.2001},
doi = {10.1128/JB.183.9.2834-2841.2001},
issn = {0021-9193},
year = {2001},
date = {2001-05-01},
urldate = {2001-05-01},
journal = {Journal of Bacteriology},
volume = {183},
number = {9},
pages = {2834-2841},
abstract = {Twelve populations of \textit{Escherichia coli} B all lost d -ribose catabolic function during 2,000 generations of evolution in glucose minimal medium. We sought to identify the population genetic processes and molecular genetic events that caused these rapid and parallel losses. Seven independent Rbs ^{−} mutants were isolated, and their competitive fitnesses were measured relative to that of their Rbs ^{+} progenitor. These Rbs ^{−} mutants were all about 1 to 2% more fit than the progenitor. A fluctuation test revealed an unusually high rate, about 5 × 10 ^{−5} per cell generation, of mutation from Rbs ^{+} to Rbs ^{−}, which contributed to rapid fixation. At the molecular level, the loss of ribose catabolic function involved the deletion of part or all of the ribose operon (\textit{rbs} genes). The physical extent of the deletion varied between mutants, but each deletion was associated with an IS\textit{150} element located immediately upstream of the \textit{rbs} operon. The deletions apparently involved transposition into various locations within the \textit{rbs} operon; recombination between the new IS\textit{150} copy and the one upstream of the \textit{rbs} operon then led to the deletion of the intervening sequence. To confirm that the beneficial fitness effect was caused by deletion of the \textit{rbs} operon (and not some undetected mutation elsewhere), we used P1 transduction to restore the functional \textit{rbs} operon to two Rbs^{−} mutants, and we constructed another Rbs^{−} strain by gene replacement with a deletion not involving IS\textit{150}. All three of these new constructs confirmed that Rbs^{−} mutants have a competitive advantage relative to their Rbs^{+} counterparts in glucose minimal medium. The rapid and parallel evolutionary losses of ribose catabolic function thus involved both (i) an unusually high mutation rate, such that Rbs^{−} mutants appeared repeatedly in all populations, and (ii) a selective advantage in glucose minimal medium that drove these mutants to fixation.},
keywords = {Correlated Responses, Genotypes and Phenotypes},
pubstate = {published},
tppubtype = {article}
}
Twelve populations of Escherichia coli B all lost d -ribose catabolic function during 2,000 generations of evolution in glucose minimal medium. We sought to identify the population genetic processes and molecular genetic events that caused these rapid and parallel losses. Seven independent Rbs − mutants were isolated, and their competitive fitnesses were measured relative to that of their Rbs + progenitor. These Rbs − mutants were all about 1 to 2% more fit than the progenitor. A fluctuation test revealed an unusually high rate, about 5 × 10 −5 per cell generation, of mutation from Rbs + to Rbs −, which contributed to rapid fixation. At the molecular level, the loss of ribose catabolic function involved the deletion of part or all of the ribose operon (rbs genes). The physical extent of the deletion varied between mutants, but each deletion was associated with an IS150 element located immediately upstream of the rbs operon. The deletions apparently involved transposition into various locations within the rbs operon; recombination between the new IS150 copy and the one upstream of the rbs operon then led to the deletion of the intervening sequence. To confirm that the beneficial fitness effect was caused by deletion of the rbs operon (and not some undetected mutation elsewhere), we used P1 transduction to restore the functional rbs operon to two Rbs− mutants, and we constructed another Rbs− strain by gene replacement with a deletion not involving IS150. All three of these new constructs confirmed that Rbs− mutants have a competitive advantage relative to their Rbs+ counterparts in glucose minimal medium. The rapid and parallel evolutionary losses of ribose catabolic function thus involved both (i) an unusually high mutation rate, such that Rbs− mutants appeared repeatedly in all populations, and (ii) a selective advantage in glucose minimal medium that drove these mutants to fixation.
Cooper V S; Bennett A F; Lenski R E
Evolution of thermal dependence of growth rate of Escherichia coli populations during 20,000 generations in a constant environment Journal Article
Evolution, vol. 55, pp. 889 - 896, 2001.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses
@article{articleb,
title = {Evolution of thermal dependence of growth rate of \textit{Escherichia coli} populations during 20,000 generations in a constant environment},
author = {Vaughn S. Cooper and Albert F. Bennett and Richard E. Lenski},
url = {https://onlinelibrary.wiley.com/doi/10.1111/j.0014-3820.2001.tb00606.x},
doi = {10.1111/j.0014-3820.2001.tb00606.x},
year = {2001},
date = {2001-01-01},
urldate = {2001-01-01},
journal = {Evolution},
volume = {55},
pages = {889 - 896},
abstract = {Twelve experimental populations of the bacterium \textit{Escherichia coli} evolved for 20,000 generations in a defined medium at 37°C. We measured their maximum growth rates across a broad range of temperatures and at several evolutionary time points to quantify the extent to which they became thermal specialists with diminished performance at other temperatures. We also sought to determine whether antagonistic pleiotropy (genetic trade-offs) or mutation accumulation (drift decay) was primarily responsible for any thermal specialization. Populations showed consistent improvement in growth rate at moderate temperatures (27-39°C), but tended to have decreased growth rate at both low (20°C) and high (41-42°C) temperatures. Most loss occurred early in the experiment, when adaptation was most rapid. This dynamic is predicted by antagonistic pleiotropy but not by mutation accumulation. Several populations evolved high mutation rates due to defects in their DNA repair, but they did not subsequently undergo a greater decrease in growth rate at thermal extremes than populations that retained low mutation rates, contrary to the acceleration of decay predicted by mutation accumulation. Antagonistic pleiotropy therefore is more likely to be responsible for the evolution of thermal specialization observed in maximum growth rate.},
keywords = {Correlated Responses},
pubstate = {published},
tppubtype = {article}
}
Twelve experimental populations of the bacterium Escherichia coli evolved for 20,000 generations in a defined medium at 37°C. We measured their maximum growth rates across a broad range of temperatures and at several evolutionary time points to quantify the extent to which they became thermal specialists with diminished performance at other temperatures. We also sought to determine whether antagonistic pleiotropy (genetic trade-offs) or mutation accumulation (drift decay) was primarily responsible for any thermal specialization. Populations showed consistent improvement in growth rate at moderate temperatures (27-39°C), but tended to have decreased growth rate at both low (20°C) and high (41-42°C) temperatures. Most loss occurred early in the experiment, when adaptation was most rapid. This dynamic is predicted by antagonistic pleiotropy but not by mutation accumulation. Several populations evolved high mutation rates due to defects in their DNA repair, but they did not subsequently undergo a greater decrease in growth rate at thermal extremes than populations that retained low mutation rates, contrary to the acceleration of decay predicted by mutation accumulation. Antagonistic pleiotropy therefore is more likely to be responsible for the evolution of thermal specialization observed in maximum growth rate.
2000
Cooper V S; Lenski R E
The population genetics of ecological specialization in evolving Escherichia coli populations Journal Article
Nature, vol. 407, no. 6805, pp. 736–739, 2000, ISSN: 0028-0836.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Fitness Trajectories, Mutation Rates
@article{Schneider2000b,
title = {The population genetics of ecological specialization in evolving \textit{Escherichia coli} populations},
author = {Vaughn S. Cooper and Richard E. Lenski},
url = {http://www.nature.com/articles/35037572},
doi = {10.1038/35037572},
issn = {0028-0836},
year = {2000},
date = {2000-10-01},
urldate = {2000-10-01},
journal = {Nature},
volume = {407},
number = {6805},
pages = {736--739},
abstract = {When organisms adapt genetically to one environment, they may lose fitness in other environments. Two distinct population genetic processes can produce ecological specialization—mutation accumulation and antagonistic pleiotropy. In mutation accumulation, mutations become fixed by genetic drift in genes that are not maintained by selection; adaptation to one environment and loss of adaptation to another are caused by different mutations. Antagonistic pleiotropy arises from trade-offs, such that the same mutations that are beneficial in one environment are detrimental in another. In general, it is difficult to distinguish between these processes. We analysed the decay of unused catabolic functions in 12 lines of \textit{Escherichia coli} propagated on glucose for 20,000 generations. During that time, several lines evolved high mutation rates. If mutation accumulation is important, their unused functions should decay more than the other lines, but no significant difference was observed. Moreover, most catabolic losses occurred early in the experiment when beneficial mutations were being rapidly fixed, a pattern predicted by antagonistic pleiotropy. Thus, antagonistic pleiotropy appears more important than mutation accumulation for the decay of unused catabolic functions in these populations.},
keywords = {Correlated Responses, Fitness Trajectories, Mutation Rates},
pubstate = {published},
tppubtype = {article}
}
When organisms adapt genetically to one environment, they may lose fitness in other environments. Two distinct population genetic processes can produce ecological specialization—mutation accumulation and antagonistic pleiotropy. In mutation accumulation, mutations become fixed by genetic drift in genes that are not maintained by selection; adaptation to one environment and loss of adaptation to another are caused by different mutations. Antagonistic pleiotropy arises from trade-offs, such that the same mutations that are beneficial in one environment are detrimental in another. In general, it is difficult to distinguish between these processes. We analysed the decay of unused catabolic functions in 12 lines of Escherichia coli propagated on glucose for 20,000 generations. During that time, several lines evolved high mutation rates. If mutation accumulation is important, their unused functions should decay more than the other lines, but no significant difference was observed. Moreover, most catabolic losses occurred early in the experiment when beneficial mutations were being rapidly fixed, a pattern predicted by antagonistic pleiotropy. Thus, antagonistic pleiotropy appears more important than mutation accumulation for the decay of unused catabolic functions in these populations.
Lenski R E; Mongold J A
Cell Size, Shape, and Fitness in Evolving Populations of Bacteria Book Chapter
Scaling in Biology, Oxford University Press, Inc., USA, 2000, ISBN: 019513141X.
Abstract | BibTeX | Tags: Cell Morphology, Correlated Responses, Demography and Ecology
@inbook{10.5555/345504.345526,
title = {Cell Size, Shape, and Fitness in Evolving Populations of Bacteria},
author = {Richard E. Lenski and Judith A. Mongold},
isbn = {019513141X},
year = {2000},
date = {2000-01-01},
urldate = {2000-01-01},
booktitle = {Scaling in Biology},
publisher = {Oxford University Press, Inc.},
address = {USA},
abstract = {There is a long and substantial history of studying allometric scaling relationships in animals and plants, which is well represented by other chapters in this volume. These studies have relevance for many fields, from cardiovascular physiology to community ecology. From the perspective of evolutionary biology, scaling relationships are important because they provide an empirical focus for investigating the tensions between structural constraints, on the one hand, and natural selection, on the other, as they vie to shape—quite literally—organisms and life histories. Despite the breadth of research on allometric scaling, those organisms at the microscopic end of the scale, especially bacteria, have been largely ignored.},
keywords = {Cell Morphology, Correlated Responses, Demography and Ecology},
pubstate = {published},
tppubtype = {inbook}
}
There is a long and substantial history of studying allometric scaling relationships in animals and plants, which is well represented by other chapters in this volume. These studies have relevance for many fields, from cardiovascular physiology to community ecology. From the perspective of evolutionary biology, scaling relationships are important because they provide an empirical focus for investigating the tensions between structural constraints, on the one hand, and natural selection, on the other, as they vie to shape—quite literally—organisms and life histories. Despite the breadth of research on allometric scaling, those organisms at the microscopic end of the scale, especially bacteria, have been largely ignored.
1996
Travisano M; Lenski R E
Long-Term Experimental Evolution in Escherichia coli. IV. Targets of Selection and the Specificity of Adaptation Journal Article
Genetics, vol. 143, no. 1, pp. 15–26, 1996, ISSN: 1943-2631.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Genotypes and Phenotypes, Parallelism and Divergence
@article{Travisano1996,
title = {Long-Term Experimental Evolution in \textit{Escherichia coli}. IV. Targets of Selection and the Specificity of Adaptation},
author = {Michael Travisano and Richard E. Lenski},
url = {https://academic.oup.com/genetics/article/143/1/15/6016887},
doi = {10.1093/genetics/143.1.15},
issn = {1943-2631},
year = {1996},
date = {1996-05-01},
urldate = {1996-05-01},
journal = {Genetics},
volume = {143},
number = {1},
pages = {15--26},
abstract = {This study investigates the physiological manifestation of adaptive evolutionary change in 12 replicate populations of \textit{Escherichia coli} that were propagated for 2000 generations in a glucose-limited environment. Representative genotypes from each population were assayed for fitness relative to their common ancestor in the experimental glucose environment and in 11 novel single-nutrient environments. After 2000 generations, the 12 derived genotypes had diverged into at least six distinct phenotypic classes. The nutrients were classified into four groups based upon their uptake physiology. All 12 derived genotypes improved in fitness by similar amounts in the glucose environment, and this pattern of parallel fitness gains was also seen in those novel environments where the limiting nutrient shared uptake mechanisms with glucose. Fitness showed little or no consistent improvement, but much greater genetic variation, in novel environments where the limiting nutrient differed from glucose in its uptake mechanisms. This pattern of fitness variation in the novel nutrient environments suggests that the independently derived genotypes adapted to the glucose environment by similar, but not identical, changes in the physiological mechanisms for moving glucose across both the inner and outer membranes.},
keywords = {Correlated Responses, Genotypes and Phenotypes, Parallelism and Divergence},
pubstate = {published},
tppubtype = {article}
}
This study investigates the physiological manifestation of adaptive evolutionary change in 12 replicate populations of Escherichia coli that were propagated for 2000 generations in a glucose-limited environment. Representative genotypes from each population were assayed for fitness relative to their common ancestor in the experimental glucose environment and in 11 novel single-nutrient environments. After 2000 generations, the 12 derived genotypes had diverged into at least six distinct phenotypic classes. The nutrients were classified into four groups based upon their uptake physiology. All 12 derived genotypes improved in fitness by similar amounts in the glucose environment, and this pattern of parallel fitness gains was also seen in those novel environments where the limiting nutrient shared uptake mechanisms with glucose. Fitness showed little or no consistent improvement, but much greater genetic variation, in novel environments where the limiting nutrient differed from glucose in its uptake mechanisms. This pattern of fitness variation in the novel nutrient environments suggests that the independently derived genotypes adapted to the glucose environment by similar, but not identical, changes in the physiological mechanisms for moving glucose across both the inner and outer membranes.
1995
Travisano M; Mongold J A; Bennett A F; Lenski R E
Experimental Tests of the Roles of Adaptation, Chance, and History Journal Article
Science, vol. 267, no. January, 1995.
Abstract | Links | BibTeX | Altmetric | Tags: Cell Morphology, Correlated Responses, Descendant Experiments, Fitness Trajectories, Historical Contingency, Methods and Miscellaneous, Parallelism and Divergence
@article{Travisano1995,
title = {Experimental Tests of the Roles of Adaptation, Chance, and History},
author = {Michael Travisano and Judith A. Mongold and Albert F. Bennett and Richard E. Lenski},
url = {https://www.science.org/lookup/doi/10.1126/science.7809610},
doi = {https://doi.org/10.1126/science.7809610},
year = {1995},
date = {1995-01-01},
urldate = {1995-01-01},
journal = {Science},
volume = {267},
number = {January},
abstract = {The contributions of adaptation, chance, and history to the evolution of fitness and cell size were measured in two separate experiments using bacteria. In both experiments, populations propagated in identical environments achieved similar fitnesses, regardless of prior history or subsequent chance events. In contrast, the evolution of cell size, a trait weakly correlated with fitness, was more strongly influenced by history and chance.},
keywords = {Cell Morphology, Correlated Responses, Descendant Experiments, Fitness Trajectories, Historical Contingency, Methods and Miscellaneous, Parallelism and Divergence},
pubstate = {published},
tppubtype = {article}
}
The contributions of adaptation, chance, and history to the evolution of fitness and cell size were measured in two separate experiments using bacteria. In both experiments, populations propagated in identical environments achieved similar fitnesses, regardless of prior history or subsequent chance events. In contrast, the evolution of cell size, a trait weakly correlated with fitness, was more strongly influenced by history and chance.
