scholarly journals Evolutionary Stalling and a Limit on the Power of Natural Selection to Improve a Cellular Module

2019 ◽  
Author(s):  
Sandeep Venkataram ◽  
Ross Monasky ◽  
Shohreh H Sikaroodi ◽  
Sergey Kryazhimskiy ◽  
Betül Kaçar
Keyword(s):  
Escherichia Coli ◽  
Natural Selection ◽  
Adaptive Evolution ◽  
Genetic Load ◽  
Performance Theory ◽  
Biological Functions ◽  
Beneficial Mutations ◽  
Translation Machinery ◽  
Adaptive Mutations ◽  
Organismal Fitness

AbstractCells consist of molecular modules which perform vital biological functions. Cellular modules are key units of adaptive evolution because organismal fitness depends on their performance. Theory shows that in rapidly evolving populations, such as those of many microbes, adaptation is driven primarily by common beneficial mutations with large effects, while other mutations behave as if they are effectively neutral. As a consequence, if a module can be improved only by rare and/or weak beneficial mutations, its adaptive evolution would stall. However, such evolutionary stalling has not been empirically demonstrated, and it is unclear to what extent stalling may limit the power of natural selection to improve modules. Here, we empirically characterize how natural selection improves the translation machinery (TM), an essential cellular module. We experimentally evolved populations of Escherichia coli with genetically perturbed TMs for 1,000 generations. Populations with severe TM defects initially adapted via mutations in the TM, but TM adaptation stalled within about 300 generations. We estimate that the genetic load in our populations incurred by residual TM defects ranges from 0.5 to 19%. Finally, we found evidence that both epistasis and the depletion of the pool of beneficial mutations contributed to evolutionary stalling. Our results suggest that cellular modules may not be fully optimized by natural selection despite the availability of adaptive mutations.

scholarly journals Evolutionary stalling and a limit on the power of natural selection to improve a cellular module

2020 ◽  
Vol 117 (31) ◽  
pp. 18582-18590 ◽  
Author(s):  
Sandeep Venkataram ◽  
Ross Monasky ◽  
Shohreh H. Sikaroodi ◽  
Sergey Kryazhimskiy ◽  
Betul Kacar
Keyword(s):  
Escherichia Coli ◽  
Natural Selection ◽  
Adaptive Evolution ◽  
Genetic Load ◽  
Performance Theory ◽  
Biological Functions ◽  
Beneficial Mutations ◽  
Translation Machinery ◽  
Adaptive Mutations ◽  
Organismal Fitness

Cells consist of molecular modules which perform vital biological functions. Cellular modules are key units of adaptive evolution because organismal fitness depends on their performance. Theory shows that in rapidly evolving populations, such as those of many microbes, adaptation is driven primarily by common beneficial mutations with large effects, while other mutations behave as if they are effectively neutral. As a consequence, if a module can be improved only by rare and/or weak beneficial mutations, its adaptive evolution would stall. However, such evolutionary stalling has not been empirically demonstrated, and it is unclear to what extent stalling may limit the power of natural selection to improve modules. Here we empirically characterize how natural selection improves the translation machinery (TM), an essential cellular module. We experimentally evolved populations ofEscherichia coliwith genetically perturbed TMs for 1,000 generations. Populations with severe TM defects initially adapted via mutations in the TM, but TM adaptation stalled within about 300 generations. We estimate that the genetic load in our populations incurred by residual TM defects ranges from 0.5 to 19%. Finally, we found evidence that both epistasis and the depletion of the pool of beneficial mutations contributed to evolutionary stalling. Our results suggest that cellular modules may not be fully optimized by natural selection despite the availability of adaptive mutations.

scholarly journals How does adaptation sweep through the genome? Insights from long-term selection experiments

2012 ◽  
Vol 279 (1749) ◽  
pp. 5029-5038 ◽  
Author(s):  
Molly K. Burke
Keyword(s):  
Genetic Variation ◽  
Natural Selection ◽  
Population Biology ◽  
De Novo ◽  
Whole Genome ◽  
Beneficial Mutations ◽  
Adaptive Mutations ◽  
Laboratory Selection ◽  
Standing Variation ◽  
New Mutations

A major goal in evolutionary biology is to understand the origins and fates of adaptive mutations. Natural selection may act to increase the frequency of de novo beneficial mutations, or those already present in the population as standing genetic variation. These beneficial mutations may ultimately reach fixation in a population, or they may stop increasing in frequency once a particular phenotypic state has been achieved. It is not yet well understood how different features of population biology, and/or different environmental circumstances affect these adaptive processes. Experimental evolution is a promising technique for studying the dynamics of beneficial alleles, as populations evolving in the laboratory experience natural selection in a replicated, controlled manner. Whole-genome sequencing, regularly obtained over the course of sustained laboratory selection, could potentially reveal insights into the mutational dynamics that most likely occur in natural populations under similar circumstances. To date, only a few evolution experiments for which whole-genome data are available exist. This review describes results from these resequenced laboratory-selected populations, in systems with and without sexual recombination. In asexual systems, adaptation from new mutations can be studied, and results to date suggest that the complete, unimpeded fixation of these mutations is not always observed. In sexual systems, adaptation from standing genetic variation can be studied, and in the admittedly few examples we have, the complete fixation of standing variants is not always observed. To date, the relative frequency of adaptation from new mutations versus standing variation has not been tested using a single experimental system, but recent studies using Caenorhabditis elegans and Saccharomyces cerevisiae suggest that this a realistic future goal.

scholarly journals Diverse phenotypic and genetic responses to short-term selection in evolving Escherichia coli populations

2015 ◽  
Author(s):  
Marcus M Dillon ◽  
Nicholas P Rouillard ◽  
Brian Van Dam ◽  
Romain Gallet ◽  
Vaughn S Cooper
Keyword(s):  
Escherichia Coli ◽  
Fitness Landscape ◽  
Single Point ◽  
Beneficial Mutations ◽  
True Nature ◽  
Term Selection ◽  
Adaptive Mutations ◽  
Fitness Effects ◽  
Genetic Responses

Beneficial mutations fuel adaptation by altering phenotypes that enhance the fit of organisms to their environment. However, the phenotypic effects of mutations often depend on ecological context, making the distribution of effects across multiple environments essential to understanding the true nature of beneficial mutations. Studies that address both the genetic basis and ecological consequences of adaptive mutations remain rare. Here, we characterize the direct and pleiotropic fitness effects of a collection of 21 first-step beneficial mutants derived from naive and adapted genotypes used in a long-term experimental evolution of Escherichia coli. Whole-genome sequencing was used to identify most beneficial mutations. In contrast to previous studies, we find diverse fitness effects of mutations selected in a simple environment and few cases of genetic parallelism. The pleiotropic effects of these mutations were predominantly positive but some mutants were highly antagonistic in alternative environments. Further, the fitness effects of mutations derived from the adapted genotypes were dramatically reduced in nearly all environments. These findings suggest that many beneficial variants are accessible from a single point on the fitness landscape, and the fixation of alternative beneficial mutations may have dramatic consequences for niche breadth reduction via metabolic erosion.

Transient and Heritable Mutators in Adaptive Evolution in the Lab and in Nature

Genetics ◽  
1998 ◽  
Vol 148 (4) ◽  
pp. 1559-1566 ◽  
Author(s):  
Susan M Rosenberg ◽  
Carl Thulin ◽  
Reuben S Harris
Keyword(s):  
Escherichia Coli ◽  
Stationary Phase ◽  
Molecular Mechanism ◽  
Adaptive Evolution ◽  
Small Proportion ◽  
Mutator Phenotype ◽  
Adaptive Mutations ◽  
Phase Mutation ◽  
New Evidence

AbstractMajor advances in understanding the molecular mechanism of recombination-dependent stationary-phase mutation in Escherichia coli occurred this past year. These advances are reviewed here, and we also present new evidence that the mutagenic state responsible is transient. We find that most stationary-phase mutants do not possess a heritable stationary-phase mutator phenotype, although a small proportion of heritable mutators was found previously. We outline similarities between this well-studied system and several recent examples of adaptive evolution associated with heritable mutator phenotype in a similarly small proportion of survivors of selection in nature and in the lab. We suggest the following: (1) Transient mutator states may also be a predominant source of adaptive mutations in these latter systems, the heritable mutators being a minority (Rosenberg 1997); (2) heritable mutators may sometimes be a product of, rather than the cause of, hypermutation that gives rise to adaptive mutations.

scholarly journals Natural selection as the process of accumulating genetic information in adaptive evolution

1961 ◽  
Vol 2 (1) ◽  
pp. 127-140 ◽  
Author(s):  
Motoo Kimura
Keyword(s):  
Natural Selection ◽  
Adaptive Evolution ◽  
Genetic Information ◽  
Genetic Load ◽  
Genetic Constitution ◽  
Linear Sequence ◽  
A Value ◽  
Darwinian Fitness ◽  
Image Position ◽  
Rate Of Accumulation

1. In the course of evolution, complicated organisms have descended from much simpler ones. Since the instructions to form an organism are contained in the nucleus of its fertilized egg, this means that the genetic constitution has become correspondingly more complex in evolution. If we express this complexity in terms of its improbability, defining the amount of genetic information as the negative logarithm of its probability of occurrence by chance, we may say that genetic information is increased in the course of progressive evolution, guided by natural selection of random mutations.2. It was demonstrated that the rate of accumulation of genetic information in adaptive evolution is directly proportional to the substitutional load, i.e. the decrease of Darwinian fitness brought about by substituting for one gene its allelic form which is more fitted to a new environment. The rate of accumulation of genetic information is given bywhere Le is the substitutional load measured in ‘Malthusian parameters’.3. Using Le = 0·199, a value obtained from the application of the ‘principle of minimum genetic load’ (cf. Kimura, 1960 b), we getIt was estimated that the total amount of genetic information accumulated since the beginning of the Cambrian epoch (500 million years) may be of the order of 108 bits, if evolution has proceeded at the standard rate.Since the genetic information is transformed into phenotypic information in ontogeny, this figure (108 bits) must represent the amount of information which corresponds to the improved organization of higher animals as compared to their ancestors 500 million years back.4. Problems involved in storage and transformation of genetic information thus acquired were discussed and it was pointed out that the redundancy of information in the form of repetition in linear sequence of nucleotide pairs within a gene may play an important role in the storage of genetic information.

scholarly journals The Evolution of Recombination: Removing the Limits to Natural Selection

Genetics ◽  
1997 ◽  
Vol 147 (2) ◽  
pp. 879-906 ◽  
Author(s):  
Sarah Perin Otto ◽  
Nick H Barton
Keyword(s):  
Natural Selection ◽  
Mutation Rate ◽  
Recombination Rate ◽  
Evolutionary Change ◽  
Fixation Probability ◽  
Beneficial Mutation ◽  
Beneficial Mutations ◽  
Adaptive Mutations ◽  
Tight Linkage ◽  
Selection For

One of the oldest hypotheses for the advantage of recombination is that recombination allows beneficial mutations that arise in different individuals to be placed together on the same chromosome. Unless recombination occurs, one of the beneficial alleles is doomed to extinction, slowing the rate at which adaptive mutations are incorporated within a population. We model the effects of a modifier of recombination on the fixation probability of beneficial mutations when beneficial alleles are segregating at other loci. We find that modifier alleles that increase recombination do increase the fixation probability of beneficial mutants and subsequently hitchhike along as the mutants rise in frequency. The strength of selection favoring a modifier that increases recombination is proportional to λ2  Sδr/r when linkage is tight and λ2  S  3δr/N when linkage is loose, where λ is the beneficial mutation rate per genome per generation throughout a population of size N, S is the average mutant effect, r is the average recombination rate, and δr is the amount that recombination is modified. We conclude that selection for recombination will be substantial only if there is tight linkage within the genome or if many loci are subject to directional selection as during periods of rapid evolutionary change.

scholarly journals Selfish Genes, Pleiotropy and the Origin of Recombination

Genetics ◽  
1998 ◽  
Vol 149 (4) ◽  
pp. 2089-2097 ◽  
Author(s):  
Jody Hey
Keyword(s):  
Natural Selection ◽  
Simple Model ◽  
Computer Simulations ◽  
Recombination Rate ◽  
Evolutionary Origin ◽  
Deleterious Mutations ◽  
Beneficial Mutations ◽  
Selfish Genes ◽  
Simple Interaction

Abstract If multiple linked polymorphisms are under natural selection, then conflicts arise and the efficiency of natural selection is hindered relative to the case of no linkage. This simple interaction between linkage and natural selection creates an opportunity for mutations that raise the level of recombination to increase in frequency and have an enhanced chance of fixation. This important finding by S. Otto and N. Barton means that mutations that raise the recombination rate, but are otherwise neutral, will be selectively favored under fairly general circumstances of multilocus selection and linkage. The effect described by Otto and Barton, which was limited to neutral modifiers, can also be extended to include all modifiers of recombination, both beneficial and deleterious. Computer simulations show that beneficial mutations that also increase recombination have an increased chance of fixation. Similarly, deleterious mutations that also decrease recombination have an increased chance of fixation. The results suggest that a simple model of recombination modifiers, including both neutral and pleiotropic modifiers, is a necessary explanation for the evolutionary origin of recombination.

scholarly journals GENETIC LOAD IN NATURAL POPULATIONS: IS IT COMPATIBLE WITH THE HYPOTHESIS THAT MANY POLYMORPHISMS ARE MAINTAINED BY NATURAL SELECTION?

Genetics ◽  
1974 ◽  
Vol 77 (3) ◽  
pp. 569-589
Author(s):  
Martin L Tracey ◽  
Francisco J Ayala
Keyword(s):  
Drosophila Melanogaster ◽  
Natural Selection ◽  
Natural Population ◽  
Natural Populations ◽  
Genetic Load ◽  
Structural Genes ◽  
Invertebrate Species ◽  
Average Proportion ◽  
Mean Fitness ◽  
The Mean

ABSTRACT Recent studies of genetically controlled enzyme variation lead to an estimation that at least 30 to 60% of the structural genes are polymorphic in natural populations of many vertebrate and invertebrate species. Some authors have argued that a substantial proportion of these polymorphisms cannot be maintained by natural selection because this would result in an unbearable genetic load. If many polymorphisms are maintained by heterotic natural selection, individuals with much greater than average proportion of homozygous loci should have very low fitness. We have measured in Drosophila melanogaster the fitness of flies homozygous for a complete chromosome relative to normal wild flies. A total of 37 chromosomes from a natural population have been tested using 92 experimental populations. The mean fitness of homozygous flies is 0.12 for second chromosomes, and 0.13 for third chromosomes. These estimates are compatible with the hypothesis that many (more than one thousand) loci are maintained by heterotic selection in natural populations of D. melanogaster.

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