- Evolution, natural selection, and genetics
- Evolution observed
- Microbial experimental evolution redux
- Evolution unlimited?
- An explosion of experimental evolution
ever since Darwin, the function of natural choice in shaping the geomorphologic, physiological, and behavioral adaptations of animals and plants across generations has been cardinal to understand life and its diverseness. New discoveries have shown with increasing preciseness how genetic, molecular, and biochemical processes produce and express those organismal features during an individual ’ sulfur life. When it comes to microorganisms, however, understanding the function of natural excerpt in producing adaptive solutions has historically been, and sometimes continues to be, contentious. This latent hostility is curious because microbes enable one to observe the ability of adaptation by natural choice with especial asperity and clarity, as exemplified by the burgeoning field of experimental microbial evolution. I trace the development of this field, describe an experiment with Escherichia coli that has been running for about 30 years, and highlight other experiments in which natural choice has led to interesting dynamics and adaptive changes in microbial populations .
Citation: Lenski RE ( 2017 ) What is adaptation by natural survival ? Perspectives of an experimental microbiologist. PLoS Genet 13 ( 4 ) : e1006668. hypertext transfer protocol : //doi.org/10.1371/journal.pgen.1006668 Editor: W. Ford Doolittle, Dalhousie University, CANADA Published: April 20, 2017
Copyright: © 2017 Richard E. Lenski. This is an overt entree article distributed under the terms of the creative Commons Attribution License, which permits nonsensitive use, distribution, and reproduction in any culture medium, provided the original generator and source are credited. Funding: REL has been supported, in character, by a National Science Foundation award ( DEB-1451740 ), the BEACON Center for the Study of Evolution in Action ( cooperative Agreement DBI-0939454 ), and the John Hannah Endowment at Michigan State University. The funders had no function in the cooking of the article. Competing interests: The writer has declared that no competing interests exist .
Evolution, natural selection, and genetics
The fields of biology and development have come a farseeing way since Charles Darwin published The Origin of Species in 1859. Nonetheless, Darwin is celebrated for the big ideas that he got right, including descent with alteration and adaptation by natural excerpt. The early refers broadly to the fact that development has occurred such that organisms living today are different from their ancestors. natural choice is the evolutionary process that explains the match, or paroxysm, between features of organisms and the environments where they live .
Jean-Baptiste Lamarck and other natural philosophers had previously put forward the theme of development in the general sense of descent with modification. And Alfred Russel Wallace, a younger contemporary of Darwin, independently came up with the concept of adaptation by natural choice. Neither outer space nor expertness allows me to do justice to the history of these ideas, except to note that Darwin is better known today than Wallace because Darwin brought to bear an extraordinary range of relevant evidence and insights that have, by and big, stood the test of time. When Darwin was rushed at the age of 50 to publish The origin by virtue of Wallace ’ second discoveries, he produced a 502-page bulk rich people with insights and details that he called a bare “ pilfer ” of the great book he had intended to publish. Over his remaining years, Darwin published many more books—The Variation of Animals and Plants Under Domestication ( 1868 ), The Descent of Man, and Selection in Relation to Sex ( 1871 ), and The Expression of the Emotions in Man and Animals ( 1872 ) among them—that provided far insights and more evidence concerning his kernel theories of descent with change and adaptation by natural choice .
Lamarck is now known largely for his hypothesis of the inheritance of acquired characteristics. While lamarckian inheritance has been soundly rejected as a general theory of biological inheritance, it seems to have foreshadowed certain especial cases in biota in which an environmental agent induces an adaptive familial change. For case, when a lysogenic bacteriophage infects a bacteria, the bacteriophage ’ s DNA can integrate into the bacterial chromosome and thereby confer immunity to reinfection by another bacteriophage. similarly, CRISPR/Cas ( clustered regularly interspaced short palindromic repeats/CRISPR-associated protein ) systems allow bacteria and archaea to incorporate bits of deoxyribonucleic acid from phages and plasmids that provide immunity against former infections [ 1 ]. cultural evolution in humans besides occurs via acquisition from the environment ( by learning ) and inheritance that is, in that deference, lamarckian. Certain maternal effects and epigenetic mechanisms are besides sometimes said to be lamarckian. however, these are extra cases and unlike from the general theory that Lamarck proposed, which has been supplanted by modern genetics and molecular biology. furthermore, these quasi-Lamarckian special cases—at least those that confer open benefits—presumably evolved by the darwinian summons of adaptation by natural choice .
But Darwin, excessively, got some things wrong. His proposed mechanism for inheritance involved “ gemmules ” made throughout the body and then concentrated in the generative organs, allowing infection across generations in a preferably lamarckian manner. Darwin besides thought the work of development was excessively slowly to directly observe. In The Origin, he wrote : “ We see nothing of these behind changes in build up, until the hand of time has marked the long sink of ages, and then therefore imperfect is our position … that we only see that the forms of life are now different from what they once were. ” This view seems rather surprising, given that The Origin began by discussing the action of domestication and using artificial excerpt as practiced by plant and animal breeders to inform the theory of natural choice. Yet even there, he wrote : “ Slow and insensible changes of this kind could never be recognised unless actual measurements or careful drawings of the breeds in question had been made long ago, which might serve for comparison. ”
The impact and scope of Darwin ’ s theories are well reflected in T. H. Huxley ’ mho wisecrack, “ How extremely stupid not to have thought of that, ” and in the title of a newspaper by Theodosius Dobzhansky [ 2 ] : “ nothing in biota makes sense except in the light of evolution. ” however, while zoologists and botanists largely embraced adaptation by natural survival following the rediscovery of mendelian inheritance and the emanation of population genetics leading to the Modern Synthesis, many microbiologists were disbelieving of its importance to the organisms they studied. For case, I. M. Lewis [ 3 ] wrote, “ The subject of bacterial magnetic declination and heredity has reached an about hopeless express of confusion … There are many advocates of the lamarckian modality of bacterial inheritance, while others hold to the watch that it is basically Darwinian. ” As a consequence, julian Huxley [ 4 ] excluded bacteria from the Modern Synthesis in 1942, writing “ They have no genes in the common sense of accurately quantal portions of ancestral substance … ”
That changed the very future class, however, when Salvador Luria and Max Delbrück [ 5 ] published their fluctuation test, which showed that mutations in E. coli that confer resistance to viruses could occur before vulnerability. That meant that natural choice was responsible for the rise in frequency of the immune mutants following photograph but not for their mutational origin. The replica-plating experiment of Joshua and Esther Lederberg [ 6 ] provided another, tied more mastermind, demonstration of the conceptual distinction between the beginning of genetic variants by mutant and the fortune of those variants, which depended on survival .
Though Darwin thought evolution was besides decelerate a process to observe directly, not all of his contemporaries agreed. In particular, William Dallinger put Darwin ’ mho theories to the test in the 1880s. An ordained minister and future president of the Royal Microscopical Society, Dallinger built an incubator in which he cultivated three protozoal species, gradually raising the temperature over several years before an accident ended the experiment [ 7, 8 ] ( Fig 1 ). Over time, new strains arose that grew at temperatures lethal to the original strains. One wonders, in retrospect, whether these strains were mutants, representatives of a diverse community present at the beginning, or possibly contaminants, although his score shows the bang-up worry with which he ran the experiment and monitored the organisms. In any case, this work showed how one could watch development in action using microorganisms. As Dallinger himself put it : “ I can only claim for this break up its suggestiveness, and its possible value as an bonus to treat the lower and minuter forms of life in corresponding manners, and as showing that such work can not be without respect. ”
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Incubator used in early on experiment on adaptation by natural survival. effigy from Dallinger ( 1887 ), now in the public domain ( hypertext transfer protocol : //commons.wikimedia.org/w/index.php ? curid=10531922 ) .
hypertext transfer protocol : //doi.org/10.1371/journal.pgen.1006668.g001 It would be many decades, however, before this value was in full realized. The experiments of Luria, Delbrück, and the Lederbergs had demonstrated that mutant and choice were distinct processes, but their main impact was in genetics, where they set off the revolution that became the field of molecular genetics by showing that microbes were superb models for understanding the physicochemical basis of heredity. however, the importance of natural choice for the “ infinitesimal forms of life ” took agree, albeit tenuously, as the result of key papers in the early 1950s .
Aaron Novick and Leo Szilard had worked on the Manhattan Project before their interests turned to biology. They sought to estimate mutant rates by measuring the rate at which phenotypically defined classes of mutants accumulated in E. coli populations growing in a chemostat, provided the mutants grew at the like rate as their parents. ( If the mutants grew more lento, as some did, they would reach a mutation–selection balance. ) Novick and Szilard [ 9, 10 ] see for a while the expected linear accretion of mutants, followed by a abrupt drop in their frequency and then a resumption of the linear increase. They hypothesized that the sudden worsen in the frequency of the observe mutants reflected an spiritual world beneficial mutation that arose in the parental background. As the fitter mutant type swept through the population, it displaced the rear stress and the discernible mutants derived from the rear. Once the fitter type had become common, then it, excessively, began to generate measurable numbers of the discernible class of mutants. Novick and Szilard tested this hypothesis by competing two strains under the same conditions : one strain bearing the discernible inert mutant isolated before the reversion, and therefore in the parental background, and the other an overlooked strain sampled after the transposition, which was hypothesized to have a beneficial mutant. As predicted, the later strain outcompeted the earlier one, and the same consequence held when the states of the achromatic mutation were reversed .
similar experiments were performed by K. C. Atwood, Lillian Schneider, and Francis Ryan [ 11, 12 ], who saw multiple selective sweeps and introduced the term “ periodic excerpt ” to describe the phenomenon. Among these early practitioners of experimental evolution, Ryan seems to have been specially smitten by the approach and its implications. In an article titled “ Evolution Observed ” for Scientific American [ 13 ], he wrote : “ And therefore the process continued : we obtained successively fitter and fitter types through 7,000 generations. All this time the metier, i, the environment, was kept changeless … It is sometimes contended that mutations can not provide the naked material for development because they are normally deleterious. But these experiments prove that survival is a mighty force for fixing and perpetuating those rare mutations that do give an advantage. ”
These insightful experiments were performed before the physical footing of heredity was known. With the discovery of the doubling coil by James Watson and Francis Crick in 1953, genetics research became dominated by molecular approaches, and experimental studies of microbial development fell largely by the wayside. As a erstwhile postdoctoral research worker with George Beadle and Edward Tatum, a mentor of Joshua Lederberg, and an active participant in the management of the Cold Spring Harbor Laboratory, Ryan was well positioned to help keep the fields of evolutionary biology and molecular genetics connected, if not united. Alas, he died in 1963 at the age of equitable 47 .
Microbial experimental evolution redux
evening as biology became increasingly split between molecular biology and “ antique ” studies ( including evolutionary biology, ecology, and studies of wholly organisms rather than their constituent molecules ), some wanderers and visionaries found fecund prime between the two camps. Carl Woese used the molecules of life to reveal the abstruse history and previously concealed diverseness of microbes [ 14 ]. Roger Milkman [ 15 ] and Robert Selander and Bruce Levin [ 16 ] followed the head of population geneticists in using molecular markers to understand the evolutionary processes that act on contemporary populations of bacteria in nature .
And still others conducted evolution experiments with microbes—sometimes to see what interesting adaptations they could produce, sometimes to better understand the dynamics of adaptation by natural selection. Patricia Clarke, Barry Hall, and Robert Mortlock [ 17 ] were leaders in the beginning group, observing how bacteria could evolve newly functions by, for case, constitutively expressing a protein with promiscuous activeness on a fresh substrate and then adapting the protein to that substrate by subsequent mutations. Using the Qβ bacteriophage, Sol Spiegelman evolved a dramatically shortened RNA genome that could self-replicate in a cell-free culture medium [ 18 ] .
On the dynamics movement, Lin Chao, Bruce Levin, and Frank Stewart studied the diversification of coevolving bacteriophage T7 and E. coli through consecutive bouts of electric resistance and host-range mutations [ 19 ]. In a report with the yeast Saccharomyces cerevisiae, Charlotte Paquin and Julian Adams showed that nontransitive competitive interactions—where B beats A, and C beats B, but A prevails against C—could lead to long-run declines in seaworthiness, even as each substitute was driven by natural choice [ 20 ]. Using different alleles of a congress of racial equality metabolic gene from natural isolates of E. coli, Daniel Dykhuizen and Daniel Hartl moved them into a common genic setting to test if they affected seaworthiness or were selectively neutral [ 21 ] .
I direct a long-run development experiment ( LTEE ) with E. coli. Six populations were founded in 1988 from each of two ancestral strains that differ by a neutral marker [ 22 ]. There are no plasmids or functional phages, and E. coli is not naturally convertible, so evolution is rigorously asexual. ad-lib mutations provide all the genic variation on which natural choice acts. The populations live in a minimal medium with glucose as the limiting resource. Every day, 1 % of each population is transferred to a flask containing clean metier, where the cells grow until they exhaust the glucose and then sit in stationary phase until the future day. The 100-fold regrowth permits ~6.7 cell generations per day. Samples of each population are sporadically stored freeze, and where they are available for late discipline. The freeze samples besides allow the populations to be restarted after accidents or disruptions. At this write, the populations have passed 66,000 generations, and the finish is to continue the experiment far into the future [ 23 ] .
I had been a postdoctoral research worker with Bruce Levin, building on his shape on coevolving bacteria and bacteriophage [ 19, 24 ]. When I started my lab, I continued working on interactions of bacteria, viruses, and plasmids, asking whether the seaworthiness costs, or tradeoffs, associated with electric resistance to viruses and antibiotics were fixed or, alternatively, could be ameliorated by compensatory adaptations [ 25, 26 ]. however, the interactions were building complex and the analyses unmanageable, so I undertook the LTEE to ask some basic questions about the process of adaptation : ( one ) What are the dynamics of adaptation by natural excerpt ? Is adaptation constantly slow and gradual ? Or are there periods of rapid change and stasis ? For how long can fitness increase ? ( two ) How repeatable is adaptive evolution ? Will replicate populations evolve along exchangeable paths ? Or will they find different solutions to identical environments ? ( three ) How are the dynamics of phenotypical and genomic evolution coupled ? What functional changes are responsible for the bacteria ’ randomness adaptation by natural choice ?
Dynamics of adaptation by natural selection
The dynamics are concern, and sometimes storm, in several respects. During the first 2,000 generations or then, the effect sizes of beneficial mutations were boastfully and produced seaworthiness trajectories with step-like dynamics [ 23, 27 ]. Over longer periods, the rate of improvement slowed substantially [ 27, 28 ]. That course might suggest that fitness is approaching some upper limit, or asymptote. however, the fitness data are good fit by a simple two-parameter power-law model, which has no asymptote, than by an evenly simpleton hyperbolic model [ 28 ]. furthermore, the power-law exemplar predicts fitness levels accurately far into the future using truncated datasets [ 28 ]. And a simple dynamic model with clonal interference ( i.e., competition between lineages with different beneficial mutations [ 29 ] ) and diminishing-returns hypostasis ( i.e., beneficial mutations confer smaller advantages in more-fit than in less-fit backgrounds ) generates a power-law relative [ 28 ] .
Repeatability of adaptation
Over 50,000 generations, a typical population increased seaworthiness by ~70 % relative to the ancestor [ 28 ], whereas a typical pair of populations differ from one another by merely a few percentage [ 30 ]. Against this backdrop of predictability, however, some populations stand out in interesting ways. half of the populations evolved hypermutable phenotypes [ 31, 32 ], which led to slightly faster rates of seaworthiness improvement [ 28, 30 ]. however, respective of those later evolve compensatory changes that reduced their mutability, reflecting the tension between the production of beneficial mutants that are the adjacent large winners and the cost of producing offspring with deleterious mutations [ 32, 33 ]. The populations besides vary in whether or not they generated stable polymorphisms that sustain diversity within them. One population has two lineages that have coexisted for over 40,000 generations [ 32, 34 ]. Their coexistence depends on crossfeeding, in which one linage is the lake superior rival for the exogenously supplied glucose and the other is better at using acetate rayon excreted into the medium [ 34, 35 ]. other LTEE populations have had transiently stable polymorphisms [ 36 ], and still others appear to have remained more homogeneous [ 32 ], although metagenomic sequence may reveal previously undetected polymorphisms .
Most strikingly, one population evolved the ability to grow on citrate at ~31,000 generations [ 37 ] ( Fig 2 ), while none of the others have done so even after 66,000 generations. Citrate has been present in the medium throughout the duration of the LTEE, where it serves as a chelate agent. In principle, citrate provides another reservoir of carbon paper and energy, but one of the defining characteristics of E. coli as a species is that it can not take up and use citrate in the presence of oxygen. Each LTEE population has tested billions of mutations over meter, so the difficulty of evolving the ability to use citrate does not reflect a scarcity of mutations ; furthermore, the population that evolved this ability was not hypermutable when it did indeed [ 38 ]. rather, the trouble of evolving this ability reflects two issues. First, expression of the relevant transporter protein required a “ promoter capture ” that involved rearranging nonhomologous deoxyribonucleic acid segments to produce a raw module [ 38 ]. Second, even with the raw module in place, effective growth on citrate requires certain other mutations in the familial background [ 37 – 40 ] .
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Experimental populations of E. coli, centered on the population that evolved the ability to use citrate in the LTEE. photograph by Brian Baer and Neerja Hajela, Michigan State University ( hypertext transfer protocol : //commons.wikimedia.org/w/index.php ? curid=4277502 ) .
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Coupling of phenotypic and genomic evolution
When the LTEE began, not a single bacterial genome had been sequenced, and for many years whole-genome sequence was excessively costly for this project. however, by working second from phenotypical changes to candidate genes and using early approaches, some mutations were discovered ; and once a mutation was found in one population, that gene was sequenced in the others [ 41 – 46 ]. This approach revealed many examples of parallel evolution at the level of genes, but because of the ad hoc ways that genes of pastime were found, it was unmanageable to assess the global extent of parallelism and the proportion of the accumulate mutations that were beneficial .
In clock time, though, it became feasible to sequence and analyze complete genomes, including, most recently, 264 clones in total from the 12 independent populations [ 32 ]. The data give an extremely strong bespeak of genomewide parallelism, with over 50 % of nonsynonymous mutations that arose in nonhypermutable lineages concentrated in just 2 % of the protein-coding genes. significant parallelism was besides seen in the hypermutable lineages, although the signal was much weaker because beneficial mutations were diluted in a larger pool of neutral and weakly deleterious mutations. While there was potent parallelism at the flat of genes, there were very few cases where the claim lapp mutations were found in any two retroflex populations. parallelism at the level of genes, and not at the level of nucleotides, supports the inference that lifelike choice, rather than mutational hotspots, drove the enrichment of the decimal point mutations. The ratio of nonsynonymous to synonymous mutations, adjusted for the number of sites at risk for each, was > 10 over the first 500 generations of the LTEE and has remained > 2 flush in late generations, providing another firm signal of natural survival [ 32 ] .
a lot work remains to be done to understand the effects of these mutations. A number have been demonstrated to be beneficial by constructing and competing genotypes that differ by specific mutations [ 47, 48 ], but how they are beneficial is much ill-defined. The genes with beneficial mutations include ones that encode proteins with core metabolic and regulative functions [ 32 ]. These genes are likely to have permeant pleiotropic and epistatic effects, contributing to the difficulty in understanding precisely how mutations in those genes benefit the cells .
An explosion of experimental evolution
The field of experimental development has grown enormously in recent years. Using the Google Ngram spectator ( hypertext transfer protocol : //books.google.com/ngrams ) for the menstruation from 1948–2008, the bible “ development ” has trended gradually up from ~0.003 % to ~0.004 %. Although used far less often, the phrase “ development experiment ” showed an ~10-fold increase in habit over that time period ( based on a 10-year run average ). It is impossible to do judge to this sphere here, but several late reviews that focus on evolution experiments using microbes are available [ 49 – 51 ]. rather, I highlight a twelve papers that illustrate the across-the-board stove of issues being studied .
several studies have documented the egress of complex interactions between bacterial genotypes derived from the lapp ancestral song. Rainey and Travisano [ 52 ] showed that populations of Pseudomonas fluorescens quickly diversified when cultured in inactive flasks but did not if the flasks were shaken. The diversification occurred because the inactive flasks generated environmental gradients, which allowed ecotypes with different environmental preferences to flourish. Zambrano et alabama. [ 53 ] starved E. coli populations and found mutants that could grow while the early cells were dying. Fiegna et aluminum. [ 54 ] studied a mutant try of Myxococcus xanthus that could produce spores entirely by exploiting other strains that made fruiting bodies. From this obligate deceiver, they evolved a strain that not only made fruiting bodies and spores on its own but that besides was insubordinate to cheating by its progenitor .
other studies have examined the development of bacteriophages and the character of host–parasite coevolution. Wichman et alabama. [ 55 ] watched two populations of bacteriophage ϕX174 evolve at senior high school temperature while growing on a novel server, Salmonella typhimurium, and then sequenced the bacteriophage genomes. They saw striking parallelism across the replicates, with about one-half of the mutations that reached eminent frequency identical at the nucleotide grade. Paterson et alabama. [ 56 ] compared the pace of development in bacteriophage ϕ2 when its P. fluorescens horde was allowed to coevolve and when the horde was prevented from evolving by repeatedly restarting it from a stock culture. They found that the bacteriophage ’ s genome evolution was faster and more varying across replicates when its host was coevolving, coherent with Red Queen dynamics. The coevolutionary dynamic between bacteriophage λ and E. coli besides enabled Meyer et alabama. [ 57 ] to select bacteriophage genotypes that could infect cells using a newly sense organ, a switch not seen in many decades of former studies of this interaction .
A different screen of coevolution—one with major health implications—occurs when humans increase antibiotic concentrations in an feat to control bacteria. A survey by Lindsey et aluminum. [ 58 ] showed that E. coli populations could sometimes be driven to extinction by raising the concentration cursorily, which prevented the bacteria from evolving the high-level resistance they reached when it was raised lento. By contrast, Baym et alabama. [ 59 ] built arenas where populations of motile E. coli evolved in a bit-by-bit fashion to grow at increasingly higher antibiotic concentrations. Their time-lapse videos provide a strike demonstration of development in action ( hypertext transfer protocol : //vimeo.com/180908160/7a7d12ead6 ) .
Some studies have used creative selection schemes to generate interest adaptations. Ratcliff et alabama. [ 60 ] performed centrifugation to select fast-settling S. cerevisiae and evolved “ snowflake ” yeast with a multicellular life history ( Fig 3 ), which in turn favors a division of labor between human body and generative cells. Most development experiments select for mutants that grow faster than their competitors, whereas many real-world applications need strains with higher yields, not faster growth. Bachmann et aluminum. [ 61 ] evolved high-yield Lactococcus lactis using a water-in-oil emulsion system. Mutants that grew more efficiently had access to the remaining resources within a droplet, thereby preventing coup d’etat by other mutants that grew faster but less efficiently .
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Clusters of “ snowflake ” yeast that evolved a multicellular life history. Confocal micrographs showing many clusters ( left ) and one at higher exaggeration ( correct ). Colors show depth in z-axis. Unpublished images by Shane Jacobeen, Will Ratcliff, and Peter Yunker, Georgia Institute of Technology .
hypertext transfer protocol : //doi.org/10.1371/journal.pgen.1006668.g003 New methods for watching the dynamics of genome evolution have besides advanced the field. Lang et alabama. [ 62 ] used metagenomic sequence to study the dynamics of within-population polymorphisms in 40 experimental populations of yeast. Levy et alabama. [ 63 ] used barcodes to track lineages in an evolve yeast population, revealing thousands of beneficial mutations that initially rose in frequency but ultimately were outcompeted by the most-fit lineage.
The studies highlighted in this short review have used microbes, but many other evolution experiments use flies, mouse, and early large organisms [ 64 ]. A few evolution experiments have even been performed not in the testing ground but in natural environments [ 65, 66 ]. And, of course, many studies of adaptation by natural excerpt take plaza without designed experiments, including the extraordinary multidecadal study of Darwin ’ mho finches in the Galápagos by Peter and Rosemary Grant [ 67 ], a well as huge swaths of comparative biota [ 68 ]. This review entirely scratches one surface of the consistency of research on adaptation by natural selection .
adaptation by natural selection has been cardinal to biology ever since Darwin presented the theme more than 150 years ago. When coupled to theories of mutant and inheritance, it explains how organism become match to their environments. Microbiologists were, on the whole, slower to accept the generalization of this theory than those who studied plants and animals. Following critical experiments that disentangled the effects of mutation and selection in microorganism, and given their short generations and big populations, experimental development has become a highly fat approach in microbiology. Some of the experiments test specific hypotheses, while others, like the LTEE, are open-ended and explore broad questions. New technologies enhance the power of experimental development, which may in turn provide new opportunities for give studies in biotechnology and medicate. As evolutionary biology continues to generate fascinate ideas and questions, experimental evolution offers one approach for examining new ideas and questions .
I thank Ford Doolittle and the american Society for Microbiology for the Jeopardy-inspired symposium that led to this article and Shane Jacobeen, Will Ratcliff, and Peter Yunker for sharing the images of the snowflake yeast .
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