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PubMed2005

Experimental evolution of Pseudomonas fluorescens in simple and complex environments.

In complex environments that contain several substitutable resources, lineages may become specialized to consume only one or a few of them. Here we investigate the importance of environmental complexity in determining the evolution of niche width over approximately 900 generations in a chemically defined experimental system. We propagated 120 replicate lines of the bacterium Pseudomonas fluorescens in environments of different complexity by using between one and eight carbon substrates in each environment. Genotypes from populations selected in complex environments evolved greater mean and variance in fitness than those from populations selected in simple environments. Thus, lineages were able to adapt to several substrates simultaneously without any appreciable loss of function with respect to other substrates present in the media. There was greater genetic and genotype-by-environment interaction variance for fitness within populations selected in complex environments. It is likely that genetic variance in populations grown on complex media was maintained because the identity of the fittest genotype varied among carbon substrates. Our results suggest that evolution in complex environments will result neither in narrow specialists nor in complete generalists but instead in overlapping imperfect generalists, each of which has become adapted to a certain range of substrates but not to all.

Bacterial Typing Techniques↗
PubMed2002

Long-term experimental evolution in Escherichia coli. XI. Rejection of non-transitive interactions as cause of declining rate of adaptation.

BACKGROUND: Experimental populations of Escherichia coli have evolved for 20,000 generations in a uniform environment. Their rate of improvement, as measured in competitions with the ancestor in that environment, has declined substantially over this period. This deceleration has been interpreted as the bacteria approaching a peak or plateau in a fitness landscape. Alternatively, this deceleration might be caused by non-transitive competitive interactions, in particular such that the measured advantage of later genotypes relative to earlier ones would be greater if they competed directly. RESULTS: To distinguish these two hypotheses, we performed a large set of competitions using one of the evolved lines. Twenty-one samples obtained at 1,000-generation intervals each competed against five genetically marked clones isolated at 5,000-generation intervals, with three-fold replication. The pattern of relative fitness values for these 315 pairwise competitions was compared with expectations under transitive and non-transitive models, the latter structured to produce the observed deceleration in fitness relative to the ancestor. In general, the relative fitness of later and earlier generations measured by direct competition agrees well with the fitness inferred from separately competing each against the ancestor. These data thus support the transitive model. CONCLUSION: Non-transitive competitive interactions were not a major feature of evolution in this population. Instead, the pronounced deceleration in its rate of fitness improvement indicates that the population early on incorporated most of those mutations that provided the greatest gains, and subsequently relied on beneficial mutations that were fewer in number, smaller in effect, or both.

Adaptation, Physiological↗
PubMed2007

Experimental evolution of gene duplicates in a bacterial plasmid model.

The fate of gene duplicates subjected to diversifying selection was tested experimentally in a bacterial system. The wild-type TEM-1 beta-lactamase gene confers resistance to ampicillin but not to cefotaxime. Point mutations confer cefotaxime resistance, but they compromise ampicillin resistance. Thus, selection for both drug resistances in a bacterium with two copies of beta-lactamase should favor the divergence of one copy to improve cefotaxime resistance while maintaining the other copy to preserve ampicillin resistance. This selection was performed on a bacterium with identical sequences of beta-lactamase on two separate, compatible plasmids. As expected, one plasmid evolved increased cefotaxime resistance when appropriately strong cefotaxime selection was applied. However, the cefotaxime-resistant plasmid maintained sufficient ampicillin resistance to tolerate the concentration of ampicillin used, and the other plasmid was lost. Hosts carrying both the cefotaxime-resistant and wild-type plasmids were then subjected to various higher concentrations of both drugs to find conditions that would ensure the maintenance of both plasmids. In a striking contradiction to our model, no such conditions were found. The fitness cost of carrying both plasmids increased dramatically as antibiotic levels were raised, and either the wild-type plasmid was lost or the cells did not grow. This study highlights the importance of the cost of duplicate genes and the quantitative nature of the tradeoff in the evolution of gene duplication through functional divergence.

Anti-Bacterial Agents↗
PubMed2005

Mutation and the experimental evolution of outcrossing in Caenorhabditis elegans.

An understanding of the forces that contribute to the phylogenetically widespread phenomenon of sexual reproduction has posed a longstanding problem in evolutionary biology. Mutational theories contend that sex can be maintained when the deleterious mutation rate is sufficiently high, although empirical evidence is equivocal and experimental studies are rare. To test the influence of mutation on the evolution of obligate outcrossing, I introduced a genetic polymorphism for breeding system into populations of the nematode Caenorhabditis elegans with high- and low-mutation rate genetic backgrounds and tracked the change in frequency of females, hermaphrodites, and males over approximately 21 generations. Hermaphrodites invaded all populations, regardless of mutational background. However, experimental populations with elevated mutation rates experienced more outcrossing and greater retention of females. This provides experimental evidence consistent with deleterious mutational explanations for the evolution of sex in principle, but the action of other processes is required to explain the evolution of sex in entirety.

Animals↗
PubMed2005

Long-term experimental evolution in Escherichia coli. XIII. Phylogenetic history of a balanced polymorphism.

We investigated the phylogenetic history of a balanced polymorphism that evolved in an experimental population of Escherichia coli. Previous work showed that two ecologically and morphologically distinct types, designated L (large) and S (small), arose by generation 6000 and coexisted for more than 12,000 generations thereafter. Here, we performed RFLP analyses using Insertion Sequence elements to resolve the phylogenetic history of L and S. Specifically, we sought to determine whether the derived S morph was monophyletic, indicating a long history of coexistence with L or, alternatively, S was repeatedly regenerated from L, indicating a series of periods with only transiently stable coexistence. Phylogenetic analysis of some 200 clones collected throughout the history of this population demonstrates that S is monophyletic. We then performed competition assays using clones of both morphs from different generations to determine whether either or both lineages continued to undergo genetic adaptation. Indeed, both lineages continued to adapt, and their continued evolution contributed to fluctuations in their relative abundance over evolutionary time. Based on their phylogenetic history and independent evolutionary trajectories, S and L fulfill Cohan's criteria for being different asexual species.

Adaptation, Physiological↗
PubMed2001

Long term adaptation of a microbial population to a permanent metabolic constraint: overcoming thymineless death by experimental evolution of Escherichia coli.

BACKGROUND: To maintain populations of microbial cells under controlled conditions of growth and environment for an indefinite duration is a prerequisite for experimentally evolving natural isolates of wild-type species or recombinant strains. This goal is beyond the scope of current continuous culture apparatus because these devices positively select mutants that evade dilution, primarily through attachment to vessel surfaces, resulting in persistent sub-populations of uncontrollable size and growth rate. RESULTS: To overcome this drawback, a device with two growth chambers periodically undergoing transient phases of sterilization was designed. The robustness of this device was assessed by propagating an E. coli strain under permanent thymine starvation for over 880 days, i.e. metabolic conditions notoriously known to lead to cell death and clogging of cultivation vessels. Ten thousand generations were required to obtain a descendant lineage that could resist thymine starvation and had recovered wild-type growth rate. CONCLUSIONS: This approach provides a technological framework for the diversification and improvement of microbial strains by long-term adaptation to inescapable metabolic constraints. An E. coli strain that is totally resistant to thymineless death was selected.

Adaptation, Physiological↗
PubMed2006

Experimental evolution with yeast.

Many of the difficulties of studying evolution in action can be surmounted using populations of microorganisms, such as yeast. A readily manipulated sexual system and an increasingly sophisticated array of molecular and genomic tools uniquely qualify Saccharomyces cerevisiae as an experimental subject. This minireview briefly describes some recent contributions of yeast experiments to current understanding of the evolution of ploidy, sex, mutation, and speciation.

Evolution, Molecular↗
PubMed1995

Catalytic consequences of experimental evolution: catalysis by a 'third-generation' evolvant of the second beta-galactosidase of Escherichia coli, ebgabcde, and by ebgabcd, a 'second-generation' evolvant containing two supposedly 'kinetically silent' mutations.

The kinetics of hydrolysis of a series of synthetic substrates by two experimentally evolved forms ('evolvants'), ebgabcd and ebgabcde, of the second beta-galactosidase of Escherichia coli have been measured. The ebgabcd enzyme differs from the wild-type (ebgo) enzyme by Asp92-->Asn (a) and Trp977-->Cys (b) changes in the large subunit, as well as two changes hitherto considered to have no kinetic effect, Ser979-->Gly in the large subunit (c) and Glu122-->Gly in the small subunit (d). The enzyme ebgabcde contains in addition a Glu93-->Lys change in the large subunit (e). Comparison of ebgabcd with ebgab [Elliott, K, Sinnott, Smith, Bommuswamy, Guo, Hall and Zhang (1992) Biochem. J. 282, 155-164] indicates that the c and d changes in fact accelerate the hydrolysis of the glycosyl-enzyme intermediate by a factor of 2.5, and also decrease the charge on the aglycone oxygen atom at the first transition state; the charge on the glycone, however, is unaltered [see K, Konstantinidis, Sinnott and Hall (1993) Biochem. J. 291, 15-17]. The e mutation causes a fall in the degalactosylation rate of about a factor of 3, and its occurrence only together with c and d mutations [Hall, Betts and Wootton (1989) Genetics 123, 635-648] suggests that degalactosylation of a hypothetical ebgabe enzyme would be so slow that the enzyme would have no biological advantage over the ancestral ebgab. The transfer products from galactosyl-ebgabcd and galactosyl-ebgabcde to high concentrations to glucose have been measured; the predominant product is allolactose, but significant quantities of lactose are also formed; however, at apparent kinetic saturation of the galactosyl-enzyme, hydrolysis rather than transfer is the preponderant pathway. A knowledge of the rates of enzyme-catalysed exchange of 18O from [1-18O]galactose to water permits the construction of the free-energy profiles for hydrolysis of lactose by begabcd and ebgabcde. As with the other evolvants, changes in the profile away from the rate-determining transition state are essentially random, and there is no correlation between the changes in the free energies of intermediates and of their flanking transition states. We consider the aggregate of our kinetic data on the ebg system to be telling experimental support for the theoretical objections of Pettersson [Pettersson (1992) Eur. J. Biochem. 206, 289-295 and previous papers] to the Albery-Knowles theory of the evolution of enzyme kinetic activity.

Catalysis↗
PubMed2000

Experimental evolution in Heterandria formosa, a livebearing fish: group selection on population size.

Group selection has historically been an important and controversial subject in evolutionary biology. There is now a compelling body of evidence, both theoretical and experimental, that group selection not only can be effective, but can be effective in situations when individual selection is not. However, experiments in which true population-level traits have been shown to evolve in response to group selection are currently limited to two species of flour beetle in the genus Tribolium and RNA viruses. Here we report the results of an experiment wherein we imposed group selection via differential extinction for increased and decreased population size at 6-week intervals, a true population-level trait, in the poeciliid fish Heterandria formosa. In contrast to most other group selection experiments, we observed no evolutionary response after six rounds of group selection in either the up- or down-selected lines. Populational heritability for population size was low, if not actually negative. Our results suggest that group selection via differential extinction may be effective only if population sizes are very small and/or migration rates are low.

Animals↗
PubMed2000

Experimental evolution recapitulates natural evolution.

Genomes of the closely related bacteriophages phiX174 and S13 are 5386 bases long and differ at 114 nucleotides, affecting 28 amino acids. Both parental phages were adapted to laboratory culture conditions in replicate lineages and analysed for nucleotide changes that accumulated experimentally Of the 126 experimental substitutions, 90% encoded amino-acid changes, and 62% of the substitutions occurred in parallel in more than one experimental line. Furthermore, missense changes at 12 of the experimental sites were at residues differing between the parental phages; in ten cases the phiX174 experimental lineages were convergent with the S13 parent, or vice versa, at both the nucleotide and amino-acid levels. Convergence at a site was even obtained in both directions in three cases. These results point to a limited number of pathways taken during evolution in these viruses, and also raise the possibility that much of the amino-acid variation in the natural evolution of these viruses has been selected.

Bacteriophage phi X 174↗
PubMed2006

High-resolution mutation mapping reveals parallel experimental evolution in yeast.

Understanding the genetic basis of evolutionary adaptation is limited by our ability to efficiently identify the genomic locations of adaptive mutations. Here we describe a method that can quickly and precisely map the genetic basis of naturally and experimentally evolved complex traits using linkage analysis. A yeast strain that expresses the evolved trait is crossed to a distinct strain background and DNA from a large pool of progeny that express the trait of interest is hybridized to oligonucleotide microarrays that detect thousands of polymorphisms between the two strains. Adaptive mutations are detected by linkage to the polymorphisms from the evolved parent. We successfully tested our method by mapping five known genes to a precision of 0.2-24 kb (0.1-10 cM), and developed computer simulations to test the effect of different factors on mapping precision. We then applied this method to four yeast strains that had independently adapted to a fluctuating glucose-galactose environment. All four strains had acquired one or more missense mutations in GAL80, the repressor of the galactose utilization pathway. When transferred into the ancestral strain, the gal80 mutations conferred the fitness advantage that the evolved strains show in the transition from glucose to galactose. Our results show an example of parallel adaptation caused by mutations in the same gene.

Algorithms↗
PubMed1997

Larger increases in sensitivity to paracatalytic inactivation than in catalytic competence during experimental evolution of the second beta-galactosidase of Escherichia coli.

Second-order rate constants (M-1.s-1) at 25 degrees C and pH 7.5 for inactivation of first-generation (ebga and ebgb), second-generation (ebgab and ebgabcd) and third-generation (ebgabcde) experimental evolvants of the title enzyme by 2',4'-dinitrophenyl 2-deoxy-2-fluoro-beta-D-galactopyranoside are 0.042, 0.30, 10, 24 and 57 respectively. Only partial inactivation is observed, except for ebgabcde. At a single high inactivator concentration, inactivation of the wild-type ebgo is also seen. The changes in sensitivity to the paracatalytic inactivator (over a range of 10(3.3)) are larger than changes in kcat/Km for lactose (over a range of 10(2.7)) or nitrophenyl galactosides (over a range of only 10(1.3)), or changes in degalactosylation rate (over a range of 10(1.7)). These data raise the possibility that evolution in the reverse sense, towards insensitivity to a paracatalytic inactivator with a proportionally lower effect on transformation of substrate, may become a mechanism for the development of bacterial resistance to antibiotics that act by paracatalytic enzyme inactivation.

Binding Sites↗
PubMed1996

Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation.

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.

Adaptation, Physiological↗
PubMed2026

Intersecting experimental evolution and CRISPR screens to identify novel toxin resistance loci.

Understanding toxin resistance in insects is key to appreciate niche adaptations but remains challenging due to its often-polygenic basis. A well-known example is the specialized association of Drosophila sechellia with noni fruit ( Morinda citrifolia ), which is toxic to most other insects, including the closely-related Drosophila simulans and Drosophila melanogaster . Toxicity of noni is due to its high concentration of octanoic acid (OA), but the mechanisms that determine sensitivity or resistance to OA in different species remain poorly understood. Here, we experimentally-evolved D. simulans with increased OA resistance, identifying multiple loci under selection. Cross-referencing these with a genome-wide, OA-resistance CRISPR screen in a D. melanogaster cell line highlighted two proteins: Kraken, a putative detoxification enzyme expressed in digestive and renal tissues, and Alkbh7, a mitochondrial protein linked to fatty acid metabolism. Both genes show elevated expression in D. sechellia and OA-resistant D. simulans . In D. melanogaster , kraken mutants are more OA-sensitive, while Alkbh7 overexpression increased OA resistance. Importantly, mutation of these genes in D. sechellia reduced OA tolerance. Our identification of genes underlying OA resistance in laboratory and natural contexts demonstrates how complementary, cross-species selection approaches can provide insights into complex mechanisms of toxin susceptibility and adaptation; such methods could also have practical applications in the characterization of natural and artificial insecticides.

Journal Article↗
PubMed2006

Reducing the cost of resistance; experimental evolution in the filamentous fungus Aspergillus nidulans.

We have studied compensatory evolution in a fludioxonil resistant mutant of the filamentous fungus Aspergillus nidulans. In an evolution experiment lasting for 27 weeks (about 3000 cell cycles) 35 parallel strains of this mutant evolved in three different environmental conditions. Our results show a severe cost of resistance (56%) in the absence of fludioxonil and in all conditions the mutant strain was able to restore fitness without loss of the resistance. In several cases, the evolved strain reached a higher fitness than the original sensitive ancestor. Fitness compensation occurred in one, two or three discrete steps. Genetic analysis of crosses between different evolved strains and between evolved and ancestral strains revealed interaction between compensatory mutations and provided information on the number of loci involved in fitness compensation. In addition, we discuss the opportunities for the experimental study of evolutionary processes provided by the filamentous fungus A. nidulans.

Aspergillus nidulans↗
PubMed1999

Experimental evolution of Ebg enzyme provides clues about the evolution of catalysis and to evolutionary potential.

The ebg (evolved beta-galactosidase) operon of Escherichia coli has been used since 1974 as a model system to dynamically study the evolutionary processes which have led to catalytic efficiency and substrate specificity in enzymes. Wild-type ebg beta-galactosidase, encoded by ebgA, is a catalytically feeble enzyme that does not hydrolyze lactose or other beta-galactosidase efficiently enough to permit growth on those substrates. Each of two specific base substitutions at widely separated sites increases catalytic activity sufficiently to permit growth, and the combination of the two mutations further increases catalytic effectiveness and expands the substrate range of the enzyme in a non-additive fashion. Experimental studies suggested that in the 3126 bp coding region those two substitutions were the only mutations capable of increasing activity toward lactose sufficiently to permit growth. Alignment of EbgA with the LacZ beta-galactosidase showed that both mutations were in active site amino acids. Multiple alignment and phylogenetic analysis of EbgA, LacZ, and 12 other related beta-galactosidases showed that EbgA and LacZ diverged from a common ancestor at least 2.2 billion years ago, that they belonged to different subclasses of the family of 14 beta-galactosidases, that the two subclasses differed at 12 of the 15 active site residues, and confirmed that the two previously identified mutations in ebgA are the only ones that can lead to enzyme with sufficient activity on lactose to permit growth. Studies of the catalytic mechanism of Ebg beta-galactosidase have allowed the widely accepted Albery and Knowles model for the evolution of catalysis to be rejected.

Amino Acid Sequence↗
PubMed2003

Experimental evolution yields hundreds of mutations in a functional viral genome.

Two lines of the bacteriophage T7 were grown to fix mutations indiscriminately, using a combination of population bottlenecks and mutagenesis. Complete genome sequences revealed 404 and 299 base substitutions in the two lines, the largest number characterized in functional microbial genomes so far. Missense substitutions outnumbered silent substitutions. Silent substitutions occurred at similar rates between essential and nonessential genes, but missense substitutions occurred at a higher rate in nonessential genes than in essential genes, as expected if they were less deleterious in the nonessential genes. Viral fitness declined during this protocol, and subsequent passaging of each mutated line in large population sizes restored some of the lost fitness. Substitution levels during these recoveries were less than 6% of those during the bottleneck phase, and only two changes during recovery were reversions of the original mutations. Exchanges of genomic fragments between the two recovered lines revealed that fitness effects of some substitutions were not additive-that interactions were accumulating which could lead to incompatibility between the diverged genomes. Based on these results, unprecedented high rates of nucleotide and functional divergence in viral genomes should be attainable experimentally by using repeated population bottlenecks at a high mutation rate interspersed with recovery.

Bacteriophage T7↗