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The suggestion that there are characteristics of living organisms that have evolved because they increase the rate of evolution is controversial and difficult to study. In this review, we examine the role that experimental evolution might play in resolving this issue. We focus on three areas in which experimental evolution has been used previously to examine questions of evolvability; the evolution of mutational supply, the evolution of genetic exchange and the evolution of genetic architecture.

In each case, we summarize what studies of experimental evolution have told us so far and speculate on where progress might be made in the future. We show that, while experimental evolution has helped us to begin to understand the evolutionary dynamics of traits that affect evolvability, many interesting questions remain to be answered. Natural selection produces organisms that are well adapted to their environment and the explanation of how complex adaptation may arise has been one of the great successes of the neo-Darwinian synthesis.

There is little doubt that the functional significance of traits as diverse as the clutch size of great tits and the infanticide behaviour of male lions can be explained in terms of their effect on an individual's genetic contribution to the future. But are there characteristics of organisms that function not to increase their fitness, but instead to increase evolvability?

That is, are there traits that are selected and maintained because they increase the ability of a population to respond to natural selection? Increasingly, the suggestion that many features of organismic design can only be understood in this context is taking hold Kirschner and Gerhart, ; Earl and Deem, However, such claims are controversial and clear evidence has been hard to come by Poole et al.

Indeed, even the term evolvability has been defined and used in different ways, from a technical measure of the amount of additive genetic variation within a population to the ability of a population to generate novel variation or acquire novel functions Kirschner and Gerhart, ; Wagner, ; Sniegowski and Murphy, Here, we define evolvability as the ability of a population to both generate and use genetic variation to respond to natural selection and an evolvability trait as a character that is selected because of its effects on evolvability.

Many features of organisms have been proposed as evolvability traits, and most can be loosely classified into one of the three categories.

First, there are characters that directly increase the input of genetic variation. The elevated mutation rate observed in many species of bacteria is one obvious example.

Similarly, there is some evidence that the existence of hypermutable domains within the genomes of pathogenic bacteria and viruses may allow more rapid adaptive responses in the face of host immune pressure Moxon et al. Second, there are characters that increase genetic variation by mixing genetic material from different lineages. The widespread existence of eukaryotic sex has been explained in this context, but genetic exchange by various mechanisms is also common place among non-eukaryotes Redfield, Third, there are characters that increase evolvability by altering the link between genotype and phenotype and so modulating the way in which a given amount of genetic variation is expressed at the phenotype level.

This category includes a diverse array of organismic features that are less easily characterized than the previous two. The modularity of organismic design, the structure of gene networks and genetic architecture and the robustness of developmental mechanisms are examples of characters that may increase evolvability in this way Wagner and Altenberg, ; Kirschner and Gerhart, ; Wagner, ; Hansen, In theory, there is nothing to preclude the selection of traits that have no other effect than to increase the evolutionary potential of a population.

However, in contrast to genes with direct effects on fitness, which respond directly to selection, evolvability genes are subject to indirect selection. Take as an example a gene that increases the genomic mutation rate, but has no other effect.

Such indirect selection will be weak in comparison to direct selection, but even weak evolutionary forces can have considerable importance over the long timescales of evolutionary history.

However, while evolvability traits are possible in theory, demonstrating that a particular trait has been shaped by such selection pressures is far from straightforward.

First, it is necessary to show that the trait really does increase the rate of adaptation. For example, increasing the supply of beneficial mutations could potentially increase the rate of adaptation, but may have little actual effect if adaptation is not limited by mutational supply. Second, it is also necessary to show that selection favours the trait because it increases evolvability rather than increased evolvability being an unselected by-product of selection for some other function Sniegowski and Murphy, This distinction between the adaptive value of a trait and its unselected consequences is critical if we are to fully understand the forces that have moulded a trait Williams, Experimental evolution offers the potential to examine directly the evolutionary dynamics of putative evolvability traits.

Such experiments allow researchers to observe directly whether a trait does indeed increase the rate of adaptation of a population, and if so, under what circumstances. In addition, it is possible to observe whether such traits increase in frequency in situations where the rate of adaptation is limiting and perhaps equally importantly, that they do not increase in frequency when it is not. In this review, we will examine some of the ways in which the techniques of experimental evolution may improve our understanding of evolvability.

We will not attempt a complete overview of the field. Instead, we begin by focusing on two areas, the evolution of elevated mutation rates in bacteria and the evolution of eukaryotic sex. These are areas in which our understanding of the evolutionary processes is reasonably well-developed, and experimental evolution studies have been central in aiding that development. We will then examine the much more controversial question of whether aspects of genetic architecture have evolved to increase evolvability Wagner, ; Hansen, This is an area that has received a great deal of attention recently, but in which our understanding is much less well-developed.

We will highlight how experimental evolution might help to develop this understanding. Adaptive evolution ultimately depends on mutation to generate the genetic variation, that is, its fuel. Thus, it seems intuitive that an organism that increases its rate of mutation might benefit from increased evolvability. This intuition is supported by theory, at least under certain conditions. Population genetic models show that in a poorly adapted population, genes that increase the genomic mutation rate termed mutators can spread by hitchhiking with the beneficial mutations that they produce Johnson, a , b ; Sniegowski et al.

However, this is much more likely to occur in organisms lacking recombination so that the association between mutator and mutation is not broken down, and is unlikely to be a significant force in sexual organisms. Naturally occurring mutator strains are found in many bacteria, including Escherichia coli. Loss-of-function mutations in DNA repair systems means that these strains have a mutation rate tofold higher than wild-type strains.

This has allowed the evolutionary dynamics of mutator genotypes to be examined in the lab. Early experiments showed that chemostats inoculated with mixtures of mutator and wild-type E. The appearance and subsequent spread to fixation of mutator alleles within 3 of the 12 long-term selection lines of the Lenski's group Sniegowski et al. Together these results provide direct evidence that genes for elevated mutation rate can spread through populations, and that they do so at a rate too high to be explained by genetic drift.

However, is increased evolvability the selective force driving the increase in frequency of these mutators or is their spread due to some other direct selective benefit? Further experiments cast doubt on a necessary link between elevated mutation rate and increased evolvability. When the rate of adaptation of mutator and wild-type E. The rate of adaptation of larger populations was limited, not by the rate of mutational supply, but by the efficiency of selection, and so elevated mutation rates had little effect Gerrish and Lenski, ; de Visser et al.

Thus, increased mutational supply does not guarantee an increase in evolvability. However, clear evidence that mutator genes can spread because they increase evolvability came from detailed examination of the three mutator lines from Lenski's experiments. In two of the three lines, the spread of the mutator genotype was accompanied by an increase in the rate of adaptation relative to populations that did not substitute mutator alleles Shaver et al.

In addition, there was no evidence that the increase in mutation rate seen was favoured by direct selection Shaver et al. However, the observed benefits of increased mutation supply are short-lived. Comparison of the fitness of the mutator populations with non-mutator lines several thousand generations later showed no measurable affect of mutator fixation on the end fitness of a population Shaver et al.

This may not be that surprising, since all of the populations had become well adapted to the simple and unchanging laboratory environment by that point, and increased evolvability offers little benefit under such conditions de Visser et al. However, this does mean that while increased evolvability may provide the adaptive explanation of why mutators increased in frequency, it does not explain their current maintenance within the populations.

The question of why these populations remain fixed for mutators in the absence of any effect on current evolvability remains to be answered Shaver et al.

Taken together, these studies provide support for the theoretical prediction that genes for elevated mutation rate can spread because they increase evolvability. However, they also show clearly how restrictive the conditions are in which this will occur and how transient such benefits can be. Such selection is unlikely to be particularly strong in natural populations, unless environmental change occurs at a high rate.

This is in line with the fact that, while mutators in many natural populations of bacteria tend to be at low frequency, they are often found at much higher frequency in pathogenic bacteria LeClerc et al. If advantages of increased mutation rate are likely to be transient in natural populations, then an organism that could increase its mutation rate with increased evolvability would be beneficial, but reduce it at other times might be at a selective advantage.

Such environment-specific modulation of mutation rates does occur in bacteria Rosenberg et al. For example, when E. The cellular machinery underlying these variable mutation rates has turned out to be remarkably complex, with several enzymes involved, allowing fine adjustments in mutation rate Metzgar and Wills, ; Jarosz et al.

The complexity of the machinery, combined with comparative evidence that it has been maintained over long evolutionary timescales and even duplicated Erill et al. However, whether it is an adaptation to increase evolvability is far from clear cut and alternative explanations have been proposed Metzgar and Wills, In particular, the increased mutation rate might simply be a consequence of changes that allow the DNA replication system to copy badly damaged DNA or DNA that cannot otherwise be copied.

Alternatively, if there is a trade-off between precision of replication and growth or survival in a stressful environment, the reduction in precision might represent a reallocation of resources. In either case, the increased evolvability would be regarded as a consequence rather than the selected function of the adaptation. Experimental evolution could potentially be used to disentangle these hypotheses. For example in E.

If it is possible to knock out this switch and manipulate the mutation rate of the standard polymerase enzymes, it will be possible to examine whether the elevated mutation rate is adaptive in the absence of an increase in the ability to copy damaged DNA.

Given the success of experimental evolution in unravelling the selective forces acting on constitutive mutators, it seems likely that it will provide a powerful tool in understanding their facultative counterparts. Coming up with experimental protocols and techniques to disentangle the selected-versus-emergent functions of the machinery that allows organisms to fine-tune their mutation rates remains a challenge for the future. Theoretical work Gerrish and Lenski, , as well as the experiments with bacteria discussed above de Visser et al.

In particular, in large populations where abundant beneficial mutations are available, adaptation may be limited by the rate at which these beneficial mutations can be fixed. In asexual populations, beneficial mutations that arise in different lineages compete with one another, and cannot be fixed together Gerrish and Lenski, This process of clonal interference is a potentially important limit on the rate of adaptation in asexual populations. The eukaryotic sexual cycle of meiosis and syngamy allows beneficial mutations that arise in different lineages to be brought together into the same individual, potentially removing the problem of clonal interference and increasing the efficiency of selection.

Indeed, the machinery involved in meiosis and syngamy appears so obviously designed to increase the variation of offspring, that for many years, it was accepted without question that the function of sex was to increase the ability of a species to evolve. More recently, this explanation has been questioned since sex carries costs to the individual that would usually be expected to outweigh any benefits to the species Maynard Smith, ; Bell, Nevertheless, more recent population genetic theory has shown that genetic modifiers for increased sex or recombination can increase in frequency because they increase the rate of adaptation Charlesworth and Barton, The modifiers are able to spread in a similar fashion to the mutators discussed above, by hitchhiking with the higher fitness genotypes that they have created.

Experiments in facultative sexual eukaryotes show clearly that sex can increase the rate of adaptation in a novel environment. In Chlamydomonas reinhardtii , even a single round of sexual reproduction can increase the rate at which a population adapts to a novel environment in the short term Colegrave et al.

Similar results have been observed in yeast, where experimentally knocking out the sexual cycle causes populations to adapt less rapidly to harsh laboratory environments Goddard et al.


Adaptive evolution of highly mutable loci in pathogenic bacteria.

Bacteria have specific loci that are highly mutable. We argue that the coexistence within bacterial genomes of such 'contingency' genes with high mutation rates, and 'housekeeping' genes with low mutation rates, is the result of adaptive evolution, and facilitates the efficient exploration of phenotypic solutions to unpredictable aspects of the host environment while minimizing deleterious effects on fitness. This site needs JavaScript to work properly. Please enable it to take advantage of the complete set of features! Clipboard, Search History, and several other advanced features are temporarily unavailable.


Experimental evolution: experimental evolution and evolvability

Either your web browser doesn't support Javascript or it is currently turned off. In the latter case, please turn on Javascript support in your web browser and reload this page. Read article at publisher's site DOI : PLoS One , 10 7 :e, 15 Jul Appl Environ Microbiol , 74 20 , 22 Aug Free to read. Mol Microbiol , 67 4 , 19 Dec


Adaptive evolution of highly mutable loci in pathogenic bacteria

Skip to search form Skip to main content You are currently offline. Some features of the site may not work correctly. DOI: Richard Moxon and Paul B. Rainey and Martin A. Nowak and Richard E.


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