Evolutionary capacitance
Encyclopedia
Just as electric capacitors store and release charge, by analogy evolutionary capacitance is the storage and release of variation. Living systems are robust
to mutations. This means that living systems accumulate genetic variation
without the variation having a phenotypic
effect. But when the system is disturbed (perhaps by stress), robustness breaks down, and the variation has phenotypic effects and is subject to the full force of natural selection
. An evolutionary capacitor is a molecular switch mechanism that can "toggle" genetic variation between hidden and revealed states. If some subset of newly revealed variation is adaptive, it becomes fixed by genetic assimilation
. After that, the rest of variation, most of which is presumably deleterious, can be switched off, leaving the population with a newly evolved advantageous trait, but no long-term handicap. For evolutionary capacitance to increase evolvability
in this way, the switching rate should not be faster than the timescale of genetic assimilation.
This mechanism would allow for rapid adaptation
to new environmental conditions. Switching rates may be a function of stress, making genetic variation more likely to affect the phenotype at times when it is most likely to be useful for adaptation. In addition, strongly deleterious variation may be purged while in a partially cryptic state, so cryptic variation that remains is more likely to be adaptive than random mutations are. Capacitance can help cross "valleys" in the fitness landscape
, where a combination of two mutations would be beneficial, even though each is deleterious on its own.
There is currently no consensus
about the extent to which capacitance might contribute to evolution in natural populations.
Switches that turn robustness to phenotypic rather genetic variation on and off do not fit the capacitance analogy, as their presence does not cause variation to accumulate over time. They have instead been called phenotypic stabilizers.
. Proteins' need to fold correctly is a big restriction on the evolution of protein sequences
. It has been proposed that the presence of chaperones may, by providing additional robustness to errors in folding, allow the exploration of a larger set of genotypes. When chaperones are overworked at times of environmental stress, this may "switch on" previously cryptic genetic variation.
. When Hsp90 is downregulated in the fruit fly Drosophila melanogaster
, a broad range of different phenotypes are seen, where the identity of the phenotype depends on the genetic background. This was thought to prove that the new phenotypes depended on pre-existing cryptic genetic variation that had merely been revealed. More recent evidence suggests that these data might be explained by new mutations caused by the reactivation of formally dormant transposable elements
. However, this finding regarding transposable elements may be dependent on the strong nature of the Hsp90 knockdown used in that experiment.
in Escherichia coli
increases mutational robustness
. This can increase evolvability
.
is a yeast
protein involved in recognising stop codon
s and causing translation
to stop correctly at the ends of proteins. Sup35p comes in a normal form ([psi-]) and a prion
form ([PSI+]). When [PSI+] is present, this depletes the amount of normal Sup35p available. As a result, the rate of errors in which translation continues beyond a stop codon increases from about 0.3% to about 1%.
This can lead to different growth rates, and sometimes different morphologies
, in matched [PSI+] and [psi-] strains in a variety of stressful environments. Sometimes the [PSI+] strain grows faster, sometimes [psi-]: this depends on the genetic background of the strain, suggesting that [PSI+] taps into pre-existing cryptic genetic variation. Mathematical models suggest that [PSI+] may have evolved, as an evolutionary capacitor, to promote evolvability
.
[PSI+] appears more frequently in response to environmental stress. In yeast, more stop codon disappearances are in-frame
, mimicking the effects of [PSI+], than would be expected from mutation bias or than are observed in other taxa that do not form the [PSI+] prion. These observations are compatible with [PSI+] acting as an evolutionary capacitor in the wild.
found that many act as phenotypic stabilizers. Knocking out a regulatory protein such as a chromatin regulator may lead to more effective capacitance than knocking out a metabolic enzyme.
mutations can be thought of as cryptic when they are present overwhelmingly in heterozygotes
rather than homozygotes. Facultative sex that takes the form of selfing can act as an evolutionary capacitor in a primarily asexual
population by creating homozygotes. Facultative sex that takes the form of outcrossing can act as an evolutionary capacitor by breaking up allele combinations with phenotypic effects that normally cancel out.
Mutational robustness
Mutational robustness describes the extent to which an organism’s phenotype remains constant in spite of mutation. Natural selection can directly induce the evolution of mutational robustness only when mutation rates are high and population sizes are large...
to mutations. This means that living systems accumulate genetic variation
Genetic variation
Genetic variation, variation in alleles of genes, occurs both within and among populations. Genetic variation is important because it provides the “raw material” for natural selection. Genetic variation is brought about by mutation, a change in a chemical structure of a gene. Polyploidy is an...
without the variation having a phenotypic
Phenotype
A phenotype is an organism's observable characteristics or traits: such as its morphology, development, biochemical or physiological properties, behavior, and products of behavior...
effect. But when the system is disturbed (perhaps by stress), robustness breaks down, and the variation has phenotypic effects and is subject to the full force of natural selection
Natural selection
Natural selection is the nonrandom process by which biologic traits become either more or less common in a population as a function of differential reproduction of their bearers. It is a key mechanism of evolution....
. An evolutionary capacitor is a molecular switch mechanism that can "toggle" genetic variation between hidden and revealed states. If some subset of newly revealed variation is adaptive, it becomes fixed by genetic assimilation
Genetic assimilation
Note: Genetic assimilation is sometimes used to describe "eventual extinction of a natural species as massive pollen flow occurs from another related species and the older crop becomes more like the new crop." This usage is unrelated to the usage below....
. After that, the rest of variation, most of which is presumably deleterious, can be switched off, leaving the population with a newly evolved advantageous trait, but no long-term handicap. For evolutionary capacitance to increase evolvability
Evolvability
Evolvability is defined as the capacity of a system for adaptive evolution. Evolvability is the ability of a population of organisms to not merely generate genetic diversity, but to generate adaptive genetic diversity, and thereby evolve through natural selection.In order for a biological organism...
in this way, the switching rate should not be faster than the timescale of genetic assimilation.
This mechanism would allow for rapid adaptation
Adaptation
An adaptation in biology is a trait with a current functional role in the life history of an organism that is maintained and evolved by means of natural selection. An adaptation refers to both the current state of being adapted and to the dynamic evolutionary process that leads to the adaptation....
to new environmental conditions. Switching rates may be a function of stress, making genetic variation more likely to affect the phenotype at times when it is most likely to be useful for adaptation. In addition, strongly deleterious variation may be purged while in a partially cryptic state, so cryptic variation that remains is more likely to be adaptive than random mutations are. Capacitance can help cross "valleys" in the fitness landscape
Fitness landscape
In evolutionary biology, fitness landscapes or adaptive landscapes are used to visualize the relationship between genotypes and reproductive success. It is assumed that every genotype has a well-defined replication rate . This fitness is the "height" of the landscape...
, where a combination of two mutations would be beneficial, even though each is deleterious on its own.
There is currently no consensus
Scientific consensus
Scientific consensus is the collective judgment, position, and opinion of the community of scientists in a particular field of study. Consensus implies general agreement, though not necessarily unanimity. Scientific consensus is not by itself a scientific argument, and it is not part of the...
about the extent to which capacitance might contribute to evolution in natural populations.
Switches that turn robustness to phenotypic rather genetic variation on and off do not fit the capacitance analogy, as their presence does not cause variation to accumulate over time. They have instead been called phenotypic stabilizers.
Chaperones
Chaperones assist in protein foldingProtein folding
Protein folding is the process by which a protein structure assumes its functional shape or conformation. It is the physical process by which a polypeptide folds into its characteristic and functional three-dimensional structure from random coil....
. Proteins' need to fold correctly is a big restriction on the evolution of protein sequences
Molecular evolution
Molecular evolution is in part a process of evolution at the scale of DNA, RNA, and proteins. Molecular evolution emerged as a scientific field in the 1960s as researchers from molecular biology, evolutionary biology and population genetics sought to understand recent discoveries on the structure...
. It has been proposed that the presence of chaperones may, by providing additional robustness to errors in folding, allow the exploration of a larger set of genotypes. When chaperones are overworked at times of environmental stress, this may "switch on" previously cryptic genetic variation.
Hsp90
The hypothesis that chaperones can act as evolutionary capacitors is closely associated with the heat shock protein Hsp90Hsp90
Hsp90 is a molecular chaperone and is one of the most abundant proteins expressed in cells. It is a member of the heat shock protein family, which is upregulated in response to stress...
. When Hsp90 is downregulated in the fruit fly Drosophila melanogaster
Drosophila melanogaster
Drosophila melanogaster is a species of Diptera, or the order of flies, in the family Drosophilidae. The species is known generally as the common fruit fly or vinegar fly. Starting from Charles W...
, a broad range of different phenotypes are seen, where the identity of the phenotype depends on the genetic background. This was thought to prove that the new phenotypes depended on pre-existing cryptic genetic variation that had merely been revealed. More recent evidence suggests that these data might be explained by new mutations caused by the reactivation of formally dormant transposable elements
Transposon
Transposable elements are sequences of DNA that can move or transpose themselves to new positions within the genome of a single cell. The mechanism of transposition can be either "copy and paste" or "cut and paste". Transposition can create phenotypically significant mutations and alter the cell's...
. However, this finding regarding transposable elements may be dependent on the strong nature of the Hsp90 knockdown used in that experiment.
GroEL
The overproduction of GroELGroEL
GroEL belongs to the chaperonin family of molecular chaperones, and is found in a large number of bacteria. It is required for the proper folding of many proteins. To function properly, GroEL requires the lid-like cochaperonin protein complex GroES...
in Escherichia coli
Escherichia coli
Escherichia coli is a Gram-negative, rod-shaped bacterium that is commonly found in the lower intestine of warm-blooded organisms . Most E. coli strains are harmless, but some serotypes can cause serious food poisoning in humans, and are occasionally responsible for product recalls...
increases mutational robustness
Mutational robustness
Mutational robustness describes the extent to which an organism’s phenotype remains constant in spite of mutation. Natural selection can directly induce the evolution of mutational robustness only when mutation rates are high and population sizes are large...
. This can increase evolvability
Evolvability
Evolvability is defined as the capacity of a system for adaptive evolution. Evolvability is the ability of a population of organisms to not merely generate genetic diversity, but to generate adaptive genetic diversity, and thereby evolve through natural selection.In order for a biological organism...
.
Yeast prion [PSI+]
Sup35pSup35p
Sup35p is the Saccharomyces cerevisiae eukaryotic translation release factor. More specifically, it is the yeast eukaryotic release factor 3 , which forms the translation termination complex with eRF1 . This complex recognizes and catalyzes the release of the nascent polypeptide chain when the...
is a yeast
Saccharomyces cerevisiae
Saccharomyces cerevisiae is a species of yeast. It is perhaps the most useful yeast, having been instrumental to baking and brewing since ancient times. It is believed that it was originally isolated from the skin of grapes...
protein involved in recognising stop codon
Stop codon
In the genetic code, a stop codon is a nucleotide triplet within messenger RNA that signals a termination of translation. Proteins are based on polypeptides, which are unique sequences of amino acids. Most codons in messenger RNA correspond to the addition of an amino acid to a growing polypeptide...
s and causing translation
Translation (genetics)
In molecular biology and genetics, translation is the third stage of protein biosynthesis . In translation, messenger RNA produced by transcription is decoded by the ribosome to produce a specific amino acid chain, or polypeptide, that will later fold into an active protein...
to stop correctly at the ends of proteins. Sup35p comes in a normal form ([psi-]) and a prion
Fungal prions
Fungal prions provide an excellent model for the understanding of disease-forming mammalian prions. Fungal prions are naturally occurring proteins that can undergo a structural conversion that becomes self-propagating and infectious. They represent an epigenetic phenomenon in which information is...
form ([PSI+]). When [PSI+] is present, this depletes the amount of normal Sup35p available. As a result, the rate of errors in which translation continues beyond a stop codon increases from about 0.3% to about 1%.
This can lead to different growth rates, and sometimes different morphologies
Morphology (biology)
In biology, morphology is a branch of bioscience dealing with the study of the form and structure of organisms and their specific structural features....
, in matched [PSI+] and [psi-] strains in a variety of stressful environments. Sometimes the [PSI+] strain grows faster, sometimes [psi-]: this depends on the genetic background of the strain, suggesting that [PSI+] taps into pre-existing cryptic genetic variation. Mathematical models suggest that [PSI+] may have evolved, as an evolutionary capacitor, to promote evolvability
Evolvability
Evolvability is defined as the capacity of a system for adaptive evolution. Evolvability is the ability of a population of organisms to not merely generate genetic diversity, but to generate adaptive genetic diversity, and thereby evolve through natural selection.In order for a biological organism...
.
[PSI+] appears more frequently in response to environmental stress. In yeast, more stop codon disappearances are in-frame
Reading frame
In biology, a reading frame is a way of breaking a sequence of nucleotides in DNA or RNA into three letter codons which can be translated in amino acids. There are 3 possible reading frames in an mRNA strand: each reading frame corresponding to starting at a different alignment...
, mimicking the effects of [PSI+], than would be expected from mutation bias or than are observed in other taxa that do not form the [PSI+] prion. These observations are compatible with [PSI+] acting as an evolutionary capacitor in the wild.
Gene knockouts
Evolutionary capacitance may also be a general feature of complex gene networks, and can be seen in simulations of gene knockouts. A screen of all gene knockouts in yeastSaccharomyces cerevisiae
Saccharomyces cerevisiae is a species of yeast. It is perhaps the most useful yeast, having been instrumental to baking and brewing since ancient times. It is believed that it was originally isolated from the skin of grapes...
found that many act as phenotypic stabilizers. Knocking out a regulatory protein such as a chromatin regulator may lead to more effective capacitance than knocking out a metabolic enzyme.
Facultative sex
RecessiveRecessive
In genetics, the term "recessive gene" refers to an allele that causes a phenotype that is only seen in a homozygous genotype and never in a heterozygous genotype. Every person has two copies of every gene on autosomal chromosomes, one from mother and one from father...
mutations can be thought of as cryptic when they are present overwhelmingly in heterozygotes
Zygosity
Zygosity refers to the similarity of alleles for a trait in an organism. If both alleles are the same, the organism is homozygous for the trait. If both alleles are different, the organism is heterozygous for that trait...
rather than homozygotes. Facultative sex that takes the form of selfing can act as an evolutionary capacitor in a primarily asexual
Asexual reproduction
Asexual reproduction is a mode of reproduction by which offspring arise from a single parent, and inherit the genes of that parent only, it is reproduction which does not involve meiosis, ploidy reduction, or fertilization. A more stringent definition is agamogenesis which is reproduction without...
population by creating homozygotes. Facultative sex that takes the form of outcrossing can act as an evolutionary capacitor by breaking up allele combinations with phenotypic effects that normally cancel out.