Richard E Lenski

Michigan State University | MSU · Department of Microbiology and Molecular Genetics

Parasites, including pathogens, can adapt to better exploit their hosts on many scales, ranging from within an infection of a single individual to series of infections spanning multiple host species. However, little is known about how the genomes of parasites in natural communities evolve when they face diverse hosts. We investigated how Bartonella...

Population bottlenecks can impact the rate of adaptation in evolving populations. On the one hand, each bottleneck reduces the genetic variation that fuels adaptation. On the other hand, each founder that survives a bottleneck can undergo more generations and leave more descendants in a resource-limited environment, which allows surviving beneficia...

Evolutionary theory seeks to explain the remarkable diversity and adaptability of life on Earth. Current theory offers substantial explanatory power, but it overlooks important transient dynamics that are prominent only when populations are outside equilibrium, such as during selective sweeps. We identify a dynamic that we call “adaptive momentum”...

The distribution of fitness effects of new mutations shapes evolution, but it is challenging to observe how it changes as organisms adapt. Using Escherichia coli lineages spanning 50,000 generations of evolution, we quantify the fitness effects of insertion mutations in every gene. Macroscopically, the fraction of deleterious mutations changed litt...

Parasites can adapt to better exploit their hosts on many timescales, ranging from within a single infection to across serial infections of multiple hosts. However, little is known about how the genomes of parasites in natural communities evolve when they face diverse hosts. We investigated how Bartonella bacteria that circulate in rodent communiti...

Background Pathogens face strong selection from host immune responses, yet many host populations support pervasive pathogen populations. We investigated this puzzle in a model system of Bartonella and rodents from Israel’s northwestern Negev Desert. We chose to study this system because, in this region, 75–100% of rodents are infected with Bartonel...

The evolution of a novel trait can profoundly change an organism's effects on its environment, which can in turn affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following the evolution of a novel function in the Long-Term Evolution Experiment (LTEE) with Escherichia coli. A characte...

The long-term evolution experiment (LTEE) with Escherichia coli began in 1988 and it continues to this day, with its 12 populations having recently reached 75,000 generations of evolution in a simple, well-controlled environment. The LTEE was designed to explore open-ended questions about the dynamics and repeatability of phenotypic and genetic evo...

Experimental evolution is an approach that allows researchers to study organisms as they evolve in controlled environments. Despite the growing popularity of this approach, there are conceptual gaps among projects that use different experimental designs. One such gap concerns the contributions to adaptation of genetic variation present at the start...

Populations of cancer cells are subject to the same core evolutionary processes as asexually reproducing, unicellular organisms. Transmissible cancers are particularly striking examples of these processes. These unusual cancers are clonal lineages that can spread through populations via physical transfer of living cancer cells from one host individ...

Experimental evolution is an approach that allows researchers to study organisms as they evolve in controlled environments. Despite the growing popularity of this approach, there are conceptual gaps among projects that use different experimental designs. One such gap concerns the contributions to adaptation of genetic variation present at the start...

Significance Populations of larger organisms should be more efficient in their resource use, but grow more slowly, than populations of smaller organisms. The relations between size, metabolism, and demography form the bedrock of metabolic theory, but most empirical tests have been correlative and indirect. Experimental lineages of Escherichia coli...

Laboratory experiments in which blood‐borne parasitic microbes evolve in their animal hosts offer an opportunity to study parasite evolution and adaptation in real time and under natural settings. The main challenge of these experiments is to establish a protocol that is both practical over multiple passages and accurately reflects natural transmis...

As evolving populations accumulate mutations, the benefits and costs of subsequent mutations change. As fitness increases, the relative benefit of new mutations typically decreases. However, the question remains whether deleterious mutations tend to have larger or smaller costs as a population adapts; theory and experiments provide support for both...

The distribution of fitness effects of new mutations is central to predicting adaptive evolution, but observing how it changes as organisms adapt is challenging. Here we use saturated, genome-wide insertion libraries to quantify how the fitness effects of new mutations changed in two E. coli populations that adapted to a constant environment for 15...

Antibiotic resistance is a growing concern that has prompted a renewed focus on drug discovery, stewardship, and evolutionary studies of the patterns and processes that underlie this phenomenon. A resistant strain’s competitive fitness relative to its sensitive counterparts in the absence of drug can impact its spread and persistence in both clinic...

Antibiotic resistance is a growing concern that has prompted a renewed focus on drug discovery, stewardship, and evolutionary studies of the patterns and processes that underlie this phenomenon. A resistant strain's competitive fitness relative to its sensitive counterparts in the absence of drug can impact its spread and persistence in both clinic...

Population bottlenecks are common in nature, and they can impact the rate of adaptation in evolving populations. On the one hand, each bottleneck reduces the genetic variation that fuels adaptation. On the other hand, each founder that survives a bottleneck can undergo more generations and leave more descendants in a resource-limited environment, w...

Body size covaries with population dynamics across lifes domains. Theory holds that metabolism imposes fundamental constraints on the coevolution of size and demography. However, studies of interspecific patterns are confounded by other factors that covary with size and demography, and experimental tests of the causal links remain elusive. Here we...

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 spa...

Bacteria often evolve resistance to phage through the loss or modification of cell surface receptors. In Escherichia coli and phage λ, such resistance can catalyze a coevolutionary arms race focused on host and phage structures that interact at the outer membrane. Here, we analyse another facet of this arms race involving interactions at the inner...

Gould had a thought experiment of replaying the tape of life that provides a conceptual framework for experiments that quantify the contributions of adaptation, chance, and history to evolutionary outcomes. For example, we can empirically measure how varying the depth of history in one environment influences subsequent evolution in a new environmen...

Bacteria often evolve resistance to phage through the loss or modification of cell-surface receptors. In Escherichia coli and phage λ, such resistance can catalyze a coevolutionary arms race focused on host and phage structures that interact at the outer membrane. Here, we analyze another facet of this arms race involving interactions at the inner...

Bacteria adopt a wide variety of sizes and shapes, with many species exhibiting stereotypical morphologies. How morphology changes, and over what timescales, is less clear. Previous work examining cell morphology in an experiment with Escherichia coli showed that populations evolved larger cells and, in some cases, cells that were less rod-like. Th...

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 addr...

Insertion sequences (IS) are ubiquitous bacterial mobile genetic elements, and the mutations they cause can be deleterious, neutral, or beneficial. The long-term dynamics of IS elements and their effects on bacteria are poorly understood, including whether they are primarily genomic parasites or important drivers of adaptation by natural selection....

Significance A fundamental question in evolution is the repeatability of adaptation. Will independently evolving populations respond similarly when facing the same environmental challenge? This question also has important public-health implications related to the growing problem of antibiotic resistance. For example, efforts to control resistance m...

A bacterium's fitness relative to its competitors, both in the presence and absence of antibiotics, plays a key role in its ecological success and clinical impact. In this study, we examine whether tetracycline-resistant mutants are less fit in the absence of the drug than their sensitive parents, and whether the fitness cost of resistance is const...

How starved bacteria adapt and multiply under replete nutrient conditions is intimately linked to their history of previous growth, their physiological state, and the surrounding environment. While automated equipment has enabled high-throughput growth measurements, data interpretation and knowledge gaps regarding the determinants of growth kinetic...

A bacterium’s fitness relative to its competitors, both in the presence and absence of antibiotics, plays a key role in its ecological success and clinical impact. In this study, we examine whether tetracycline-resistant mutants are less fit in the absence of the drug than their sensitive parents, and whether the fitness cost of resistance is const...

Antibiotic resistance is a growing health concern. Efforts to control resistance would benefit from an improved ability to forecast when and how it will evolve. Epistatic interactions between mutations can promote divergent evolutionary trajectories, which complicates our ability to predict evolution. We recently showed that differences between gen...

Bacteria adopt a wide variety of sizes and shapes, with many species exhibiting stereotypical morphologies. How morphology changes, and over what timescales, is less clear. Previous work examining cell morphology in an experiment with Escherichia coli showed that populations evolved larger cells and, in some cases, cells that were less rod-like. Th...

Fitness tradeoffs play important roles in the evolution of organisms and communities. One such tradeoff often occurs when bacteria become resistant to phage at the cost of reduced competitiveness for resources. Quantifying the cost of phage resistance has frequently relied on measuring specific traits of interest to industrial applications. In an e...

Life often follows a peculiar and winding path. This paper connects some events in my life with how I got to know Erik Goodman and how the BEACON Center for the Study of Evolution in Action came into being. Some of these events are from memory, while others were recorded in emails. Of course, BEACON has had many participants and so there are many n...

Predicting ecological and evolutionary dynamics is challenging because the phenomena of interest emerge from complex nonlinear interactions between genomes, organisms, and environments. Complexity theory predicts that small changes in a basal element of an ecosystem can impact higher-order features such as population dynamics and biodiversity. Here...

Experimental studies of evolution using microbes have a long tradition, and these studies have increased greatly in number and scope in recent decades. Most such experiments have been short in duration, typically running for weeks or months. A venerable exception, the long-term evolution experiment (LTEE) with Escherichia coli has continued for 30...

Bacterial growth in nutrient-rich and starvation conditions is intrinsically tied to the environmental history and physiological state of the population. While high-throughput technologies have enabled rapid analyses of mutant libraries, technical and biological challenges complicate data collection and interpretation. Here, we present a framework...

A bstract 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 respons...

Evolutionary innovations allow populations to colonize new ecological niches. We previously reported that aerobic growth on citrate (Cit⁺) evolved in an Escherichia coli population during adaptation to a minimal glucose medium containing citrate (DM25). Cit⁺ variants can also grow in citrate-only medium (DM0), a novel environment for E. coli. To st...

Evolutionary innovations allow populations to colonize new ecological niches. We previously reported that aerobic growth on citrate (Cit⁺) evolved in an Escherichia coli population during adaptation to a minimal glucose medium containing citrate (DM25). Cit⁺ variants can also grow in citrate-only medium (DM0), a novel environment for E. coli. To st...

Evolutionary innovations allow populations to colonize new ecological niches. We previously reported that aerobic growth on citrate (Cit⁺) evolved in an Escherichia coli population during adaptation to a minimal glucose medium containing citrate (DM25). Cit⁺ variants can also grow in citrate-only medium (DM0), a novel environment for E. coli. To st...

Evolutionary innovations allow populations to colonize new, previously inaccessible ecological niches. We previously reported that aerobic growth on citrate (Cit +) evolved in a population of Escherichia coli during adaptation to a minimal glucose medium containing citrate (DM25). Cit + can grow in citrate-only medium (DM0), which is a novel enviro...

This edited research monograph brings together contributions from computer scientists, biologists, and engineers who are engaged with the study of evolution and how it may be applied to solve real-world problems. It also serves as a Festschrift dedicated to Erik D. Goodman, the founding director of the BEACON Center for the Study of Evolution in Ac...

Evolution provides a creative fount of complex and subtle adaptations that often surprise the scientists who discover them. However, the creativity of evolution is not limited to the natural world: Artificial organisms evolving in computational environments have also elicited surprise and wonder from the researchers studying them. The process of ev...

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 restoratio...

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 restoratio...

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 t...

Transcription regulatory networks (TRNs) are of central importance for both short-term phenotypic adaptation in response to environmental fluctuations and long-term evolutionary adaptation, with global regulatory genes often being targets of natural selection in laboratory experiments. Here, we combined evolution experiments, whole-genome resequenc...

A biochemist's crusade to overturn evolution misrepresents theory and ignores evidence

Replaying the tape of life The evolutionary biologist Stephen Jay Gould once dreamed about replaying the tape of life in order to identify whether evolution is more subject to deterministic or contingent forces. Greater influence of determinism would mean that outcomes are more repeatable and less subject to variations of history. Contingency, on t...

Open-ended evolution researchers seek to create systems that continually produce new evolutionary outcomes, attempting to reflect the power and diversity of evolution in nature. The specific metrics used (novelty, complexity, diversity, etc) vary by researcher, but the holy grail would be a system where any of these can accumulate indefinitely. Of...

Open-ended evolution researchers seek to create systems that continually produce new evolutionary outcomes, attempting to reflect the power and diversity of evolution in nature. The specific metrics used (novelty, complexity, diversity, etc) vary by researcher, but the holy grail would be a system where any of these can accumulate indefinitely. Of...

Open-ended evolution researchers seek to create systems that continually produce new evolutionary outcomes, attempting to reflect the power and diversity of evolution in nature. The specific metrics used (novelty, complexity, diversity, etc) vary by researcher, but the holy grail would be a system where any of these can accumulate indefinitely. Of...

Evolutionary biology and economics are both rich in theory and steeped in data, but they also share challenges including the fact that the systems they seek to understand are, in certain respects, unique and not easily manipulated. Nonetheless, both fields have seen growing efforts to provide experimental approaches to address specific issues. Here...

Biological evolution provides a creative fount of complex and subtle adaptations, often surprising the scientists who discover them. However, because evolution is an algorithmic process that transcends the substrate in which it occurs, evolution's creativity is not limited to nature. Indeed, many researchers in the field of digital evolution have o...

Few experimental studies have examined the role that sexual recombination plays in bacterial evolution, including the effects of horizontal gene transfer on genome structure. To address this limitation, we analyzed genomes from an experiment in which Escherichia coli K-12 Hfr (high frequency recombination) donors were periodically introduced into 1...

The Ara+1 population at generation 1200 of the STLE continuation contains the F plasmid, as does the Ara–3 population. The Ara+1 and Ara–3 populations are shown in red, and all other populations in black. This plot shows the coverage distribution over the plasmid reference sequence for the initial (generation 1000) and final (generation 1200) sampl...

Calculation of lengths of donor and recipient segments in recombinant genomes. (PDF)

REL4397 and REL4398 are recombinant clones from STLE population Ara–3 that were previously studied by Turner et al. (1996). That paper found a cross-feeding interaction between these clones, which puzzlingly had declined in fitness relative to their progenitor during the STLE. The REL606 genomic coordinates are shown on the x-axis, centered on the...

Recombinant clones from STLE population Ara–3 only contain the F plasmid. Read coverage over the plasmid reference sequence is plotted for each STLE recombinant clone. The spikes in read coverage near the start and near 20 Kbp of the plasmid reference are false-positive reads that map onto repeat sequences in the plasmid. (A) All Ara–3 STLE clones...

Sequence divergence between donors and recipients does not appreciably affect introgression efficiency, but it does affect the location of recombination breakpoints. The recipients are all recently derived from REL606, itself a derivative of E. coli B. The REL606 genome is 4,629,812 bp, which we divided into 556 bins that are each 8327 bp long. Eac...

Parallel fixations of K-12 genetic markers during the STLE. K-12 markers found in both recombinant clones and at 100% frequency in both the initial (1000 generation) and final (1200 generation) samples of the STLE continuation experiment were summed over each population (omitting the Ara–3 population which is almost completely derived from K-12 don...

The identifying numbers and relationships of the 12 sequenced recipient clones used to start the 12 STLE populations and the 24 recombinant clones isolated at the end of the STLE. (XLSX)

Population samples used in the STLE continuation and subsequent sequencing. (XLSX)

Histogram of the density of K-12 specific markers plotted along the genome coordinates of REL606, the ancestral strain of the LTEE. The numbers were binned over 556 DNA segments that are each 8327 bp in length. (PDF)

Whole-protein alignments of proteins encoded by genes in which mutations present in the recipient were replaced by donor DNA in the odd-numbered STLE recombinant clones. (TXT)

Genome structure of even-numbered clones from recombinant populations after 1000 generations of the STLE. The REL606 genomic coordinates are shown on the x-axis, centered on the oriC origin of replication, and the source populations are shown on the y-axis. Genetic markers are shown as vertical lines, with the color indicating the origin of each ma...

Evolution is the central unifying concept of modern biology. However, evolution requires changes over generational time, making it difficult to investigate in many taxa. Microbial systems therefore offer an unparalleled opportunity to study evolution in an experimental setting. Here, we review some of the fundamental concepts in evolutionary biolog...

The outcomes of evolution are determined by a stochastic dynamical process that governs how mutations arise and spread through a population. However, it is difficult to observe these dynamics directly over long periods and across entire genomes. Here we analyse the dynamics of molecular evolution in twelve experimental populations of Escherichia co...

The fitness effects of mutations can depend on the genetic backgrounds in which they occur and thereby influence future opportunities for evolving populations. In particular, mutations that fix in a population might change the selective benefit of subsequent mutations, giving rise to historical contingency. We examine these effects by focusing on m...