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Evidence for the Adaptive Evolution Minireview of Mutation Rates Cell, Vol. 101, 581±584, June 9, 2000, Copyright 2000 by Cell Press Evidence for the Adaptive Evolution Minireview of Mutation Rates David Metzgar*³ and Christopher Wills*² under starvation conditions in Escherichia coli (Rosen- *Department of Biology berg et al., 1998). Loss-of-function mutations in genes ² Center for Molecular Genetics required for growth can back-mutate, allowing survival University of California, San Diego and reproduction. The rate of these back-mutations (as La Jolla, California 92093 well as of other, nonadaptive mutations) increases greatly with starvation. This mutator phenotype is not itself heritableÐthe survivors produce progeny cells Adaptive evolution has long been regarded as the result with normal mutation rates. of postmutational sorting by the process of natural se- The SOS response has been implicated in such adap- lection. Mutations have been postulated to occur at ran- tive mutation (Rosenberg et al., 1998). The SOS system dom, producing genetically different individuals that is a DNA repair mechanism induced when the E. coli then compete for resources, the result being selection genome suffers physical damage such as double-strand of better adapted genotypes. Molecular biology has breaks, and can be triggered by starvation. It includes demonstrated, however, that the rate and spectrum of alternative DNA polymerase enzymes, such as DinB and mutations is in large part under the control of genetic the UmuDЈ2C complex, which are capable of replicating factors. Because genetic factors are themselves the badly damaged sequences. In the process of repair, subject of adaptive evolution, this discovery has brought these alternative polymerases generate mutations at a into question the random nature of mutagenesis. It high rate. DinB is known to generate mutations at un- would be highly adaptive for organisms inhabiting vari- damaged sites when SOS is induced. It has been sug- able environments to modulate mutational dynamics in gested that DinB and similar enzymes have evolved to ways likely to produce necessary adaptive mutations in produce genome-wide genetic variation under stressful a timely fashion while limiting the generation of other, conditions, allowing organisms to adapt rapidly when probably deleterious, mutations. necessary (Radman, 1999). Homologs of these alterna- Have genetic systems emerged that tune mutation tive polymerases with similar functions have been identi- rates and spectra in adaptive ways? Such tuning would fied in Saccharomyces cerevisiae, and homologs have produce mutations with a greater chance of being adap- also been identified by sequence similarity in mice and tive than if they were completely random. This possibility humans (for review see Friedberg and Gerlach, 1999). has met with resistance from theorists who point out that Another potential mechanism for generating variation such systems may violate a basic tenet of evolutionary under stressful conditions has been recently described theoryÐevolution does not involve foresight (Dickenson in a eukaryote. Some of the genetic variation that is and Seger, 1999). Here, we review recent evidence for capable of affecting development in Drosophila is masked the existence of adaptively tuned mutation rates. We under normal circumstances. This masking is accom- conclude that these mechanisms do not require any plished by the chaperone properties of the heat-shock special foresight. Instead, they must have been selected protein Hsp90. This protein stabilizes signal transduc- for repeatedly in the past for their ability to generate tion factors that regulate development. Mutational or genetic change. Mutational tuning does not require the pharmacological impairment of Hsp90 reveals otherwise specific generation of adaptive mutations (nonran- unexpressed developmental variation (Rutherford and domness with respect to function) but rather the con- Lindquist, 1998). These laboratory manipulations mimic centration of mutations under specific environmental the potential effects of heat stress or other protein- conditions or in particular regions of the genome (non- damaging conditions in the natural environment, condi- randomness with respect to time or location). Given a tions under which Hsp90 is diverted from the proteins predictably variable environment, adaptively tuned mu- it normally stabilizes to other environmentally denatured tation rates can evolve in ways completely consistent proteins. Exposed developmental variants can be fixed with the modern synthetic theory of evolution. in the population by selection. Changes in mutation rate can be either environment Environment-dependent mutators operate when ge- dependent or heritable. Environment-dependent changes netic change is necessary (when the organism is mal- result from induction or suppression of mutator mecha- adapted to its current environment). Moreover, the off- nisms that are present in all individuals and that have spring are not saddled with an increased rate of global (genome-wide) effects on mutation rate. Heritable deleterious mutation. The essential evolutionary ques- mutator mechanisms are independent of the environ- tion is this: did systems such as SOS and Hsp90 evolve ment. They may act by altering the global mutation rate to produce or reveal genetic variation under stress, or or they may be local, taking the form of gene sequences is this potentially adaptive property an accidental by- that experience unusually high or low rates of specific product of other factors? types of mutation. Such an evolutionary accident has been termed a Environment-Dependent Mutators spandrel, by analogy with the spaces (spandrels) that Environment-dependent global mutators are responsi- result whenever a round dome is supported by a square ble for adaptive mutations of the type that are produced formed by four arches. These spaces were secondarily used as aesthetically stunning venues for mosaic por- ³ To whom correspondence should be addressed (e-mail: traits in St. Mark's Cathedral and other buildings. Al- [email protected]). though they provide an optimal form for these mosaics, Cell 582 Figure 1. General Model of Functional Variability Driven by Hypermutable Microsatellites in Prokaryotic Contingency Loci Antigen- and phase-determinant genes containing nontriplet microsatellites turn on and off at high rates due to replication slippage mutations that cause repeat-number changes in the microsatellite. These mutations occur at very high rates (␮ Ϸ 10-3). it was not their original purpose. In evolutionary termi- Yersinia (Najdenski et al., 1995) have demonstrated posi- nology, the adaptive use of a function selected for an- tive correlations between global mutation rates and viru- other purpose is known as an exaptation. lence. Bacterial mutator phenotypes have been traced The DNA polymerases involved in SOS-associated to mutations in DNA repair genes, particularly the mutagenesis are, by necessity, less specific than their methyl-directed mismatch repair (MMR) system. Muta- constitutive counterparts. They must be able to copy tors have also been found in HIV reverse transcriptase. DNA that is so severely damaged that it interferes with The fixation of heritable global mutator systems re- the action of higher-fidelity constitutive polymerases. quires second-order selection; the mutator can only be Indeed, the mutations introduced by the SOS-associ- spread through the population through the production of ated UmuDЈ2C are the result of repair activities. The linked advantageous mutations (Weber, 1996). Second- tendency for DinB to introduce mutations at undamaged order selection is facilitated by asexual reproduction, sites may also be a consequence of low fidelity that which maintains linkage. evolved to facilitate repair. Thus, the apparently adap- Both laboratory experiments and modeling studies tive hypermutagenesis of the SOS response may simply have shown that increased rates of mutation are only be a spandrelÐthe byproduct of functions evolved for favored when the normal mutation rate is the limiting repair. factor in adaptation and when the selective advantage Similarly, it is impossible to tell whether the Hsp90 of possible adaptive mutations is high (deVisser et al., system evolved under selective pressure to limit devel- 1999). Pathogenic prokaryotes may be in a particularly opmental variability in the absence of stress, to provide good position to take advantage of mutator phenotypes. variability in the presence of stress, or both. It is not Their populations experience extreme bottlenecks that clear whether any of the variability revealed under stress reduce existing genetic variability, and individual muta- through the action (or inaction) of Hsp90 is of a poten- tions can have exceptional advantages. Nonetheless, in tially adaptive nature nor has the ability of heat-stressed asexual populations there is a limit to the contribution flies to adapt more rapidly to environmental changes that increases in mutation rate can make to the rate of been tested under circumstances designed to mimic adaptation. This is because multiple adaptive mutants natural adaptation. coexisting in the same asexual population but in differ- Heritable Global Mutators ent individuals cannot be simultaneously brought to fixa- Heritable global mutators have been detected in short- tion. They compete with each other for fixation, a phe- and long-term laboratory selection experiments (Snie- nomenon known as clonal interference (deVisser et al., gowski et al., 1997; Miller
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