Evolutionary capacitance

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Evolutionary capacitance is the storage and release of variation, just as electric capacitors store and release charge. 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. [1] 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. [2]

Contents

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. [3] 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. [2] [3] [4]

There is currently no consensus about the extent to which capacitance might contribute to evolution in natural populations. The possibility of evolutionary capacitance is considered to be part of the extended evolutionary synthesis. [5]

Switches that turn robustness to phenotypic rather than 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. [6]

Enzyme promiscuity

In addition to their native reaction, many enzymes perform side reactions. [7] Similarly, binding proteins may spend some proportion of their time bound to off-target proteins. These reactions or interactions may be of no consequence to current fitness but under altered conditions, may provide the starting point for adaptive evolution. [8] For example, several mutations in the antibiotic resistance gene B-lactamase introduce cefotaxime resistance but do not affect ampicillin resistance. [9] In populations exposed only to ampicillin, such mutations may be present in a minority of members since there is not fitness cost (i.e. are within the neutral network). This represents cryptic genetic variation since if the population is newly exposed to cefotaxime, the minority members will exhibit some resistance.

Chaperones

Chaperones assist in protein folding. The need to fold proteins 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. [10]

Hsp90

The hypothesis that chaperones can act as evolutionary capacitors is closely associated with the heat shock protein Hsp90. 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. [10] Also, a recent study on the model insect, the red flour beetle Tribolium castaneum, showed that Hsp90 impairment revealed a new phenotype, reduced-eye phenotype, which was stably inherited without further HSP90 inhibition (https://doi.org/10.1101/690727). 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. [11] However, this finding regarding transposable elements may be dependent on the strong nature of the Hsp90 knockdown used in that experiment. [12]

GroEL

The overproduction of GroEL in Escherichia coli increases mutational robustness. [13] This can increase evolvability. [14]

Yeast prion [PSI+]

Sup35p is a yeast protein involved in recognising stop codons 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%. [15]

This can lead to different growth rates, and sometimes different morphologies, in matched [PSI+] and [psi-] strains in a variety of stressful environments. [16] 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. [17] [18]

[PSI+] appears more frequently in response to environmental stress. [19] 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. [20] These observations are compatible with [PSI+] acting as an evolutionary capacitor in the wild.

Similar transient increases in error rates can evolve emergently in the absence of a "widget" like [PSI+]. [21] The primary advantage of a [PSI+]-like widget is to facilitate the subsequent evolution of lower error rates once genetic assimilation has occurred. [22]

Gene knockouts

Gene knockouts can be used to identify novel genes or genomic regions which function as evolutionary capacitors. When a gene is knocked out, and its removal reveals phenotypic variation that was not previously observable, that gene is functioning as a phenotypic capacitor. If any of the variation is adaptive, it is functioning as an evolutionary capacitor.

Fruit Flies

Deficiency in at least 15 different genes reveals cryptic variation in wing morphology in Drosophila melanogaster. While some of the variation revealed by these knockouts is deleterious, other variation has a relatively minor effect on aerodynamics, and could even improve the flight capability of an individual. [23]

Yeast

In yeast, the knockout of certain chromatin regulating genes increases the differences in expression between yeast species. The majority of the variation in protein expression is attributable to trans effects, suggesting that trans-regulatory processes are strongly involved in canalization. Unlike the chromatin regulators, the removal of genes which code for metabolic enzymes does not have a consistent effect on the difference in expression between species, with different enzyme knockouts either increasing, decreasing, or not significantly affecting the expression difference. [24]

Broader knockout samples in yeast have identified at least 300 genes which, when absent, increase morphological variation between yeast individuals. These capacitor genes predominantly occupy a few key domains in gene ontology, including chromosome organization and DNA integrity, RNA elongation, protein modification, cell cycle, and response to stimuli such as stress. More generally, capacitor genes are likely to express proteins which act as network hubs in the interactome of a cell, and in the network of synthetic-lethal interactions. The confidence that a specific gene acts as a phenotypic capacitor is correlated with the number of protein-protein interactions observed for its expressed protein. However, proteins with the highest amount of interactions have reduced phenotypic capacitance, possibly due to increased duplication of regions coding these proteins in the genome, reducing the effect of a single knockout.

Singleton capacitors (light blue) are generally part of large complexes, while duplicate capacitors (dark blue) often interact with several major complexes. Singleton and Duplicate Capacitor Genes in Yeast.jpg
Singleton capacitors (light blue) are generally part of large complexes, while duplicate capacitors (dark blue) often interact with several major complexes.

Capacitor genes are less likely to have paralogs elsewhere in the genome; most capacitors identified in yeast are either singleton genes, or have historical paralogs from which they have diverged substantially in terms of expression. Singleton and duplicate capacitors largely exhibit disjoint behavior in the interactome. Singleton capacitors are most often part of highly interconnected complexes (such as the mediator complex), while duplicate capacitors are more highly connected and tend to interact with multiple large complexes. The gene ontologies of singleton and duplicate capacitors also differ notably. Singleton capacitors are concentrated in the categories of DNA maintenance and organization, response to stimuli, and RNA transcription and localization, whereas duplicate capacitors are concentrated in the categories of protein metabolism and endocytosis. [25]

Redundancy

The mechanism of phenotypic capacitor genes in yeast appears to be closely related to the modalities of functional redundancy at various levels of the genome. Coding regions that are necessary for the synthesis of key proteins which do not have paralogs elsewhere in the genome are lethal when removed. Conversely, coding regions with many paralogs or strongly expressed paralogs have a minimal effect on overall expression (especially trans regulatory expression) when removed. Singleton and duplicate capacitors both largely represent instances of incomplete functional redundancy; differentially expressed paralogs of duplicate capacitors continue some functionality of the original gene, and the protein-protein interaction complexes within which singleton capacitors reside largely exhibit overlapping functionality. In general the phenotypic capacitors identified by knockouts in yeast are genes expressed in several key regulatory areas which, while non-lethal when removed, do not have enough redundancy to maintain complete functionality. The concept of functional redundancy may also be involved in the high number of synthetic-lethal interactions which capacitor genes participate in. When a gene has its functionality resumed by a paralog or functional analog, its removal is not inherently lethal, however when the gene and its redundancy are removed, the result is lethality.

Simulations

Computational simulations of knockouts in complex gene interaction networks have demonstrated that many, and possibly all expressed genes have the potential to reveal phenotypic variation of some kind when removed, and that previously identified capacitor genes are simply especially strong examples. Capacitance, then, is simply a feature of complex gene networks that arises in conjunction with canalization. [26]

Facultative sex

Recessive 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. [27] 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. [28]

See also

Related Research Articles

<span class="mw-page-title-main">Mutation</span> Alteration in the nucleotide sequence of a genome

In biology, a mutation is an alteration in the nucleic acid sequence of the genome of an organism, virus, or extrachromosomal DNA. Viral genomes contain either DNA or RNA. Mutations result from errors during DNA or viral replication, mitosis, or meiosis or other types of damage to DNA, which then may undergo error-prone repair, cause an error during other forms of repair, or cause an error during replication. Mutations may also result from insertion or deletion of segments of DNA due to mobile genetic elements.

<span class="mw-page-title-main">Phenotype</span> Composite of the organisms observable characteristics or traits

In genetics, the phenotype is the set of observable characteristics or traits of an organism. The term covers the organism's morphology, its developmental processes, its biochemical and physiological properties, its behavior, and the products of behavior. An organism's phenotype results from two basic factors: the expression of an organism's genetic code and the influence of environmental factors. Both factors may interact, further affecting the phenotype. When two or more clearly different phenotypes exist in the same population of a species, the species is called polymorphic. A well-documented example of polymorphism is Labrador Retriever coloring; while the coat color depends on many genes, it is clearly seen in the environment as yellow, black, and brown. Richard Dawkins in 1978 and then again in his 1982 book The Extended Phenotype suggested that one can regard bird nests and other built structures such as caddisfly larva cases and beaver dams as "extended phenotypes".

<span class="mw-page-title-main">Epigenetics</span> Study of DNA modifications that do not change its sequence

In biology, epigenetics is the study of heritable traits, or a stable change of cell function, that happen without changes to the DNA sequence. The Greek prefix epi- in epigenetics implies features that are "on top of" or "in addition to" the traditional genetic mechanism of inheritance. Epigenetics usually involves a change that is not erased by cell division, and affects the regulation of gene expression. Such effects on cellular and physiological phenotypic traits may result from environmental factors, or be part of normal development. They can lead to cancer.

<span class="mw-page-title-main">Susan Lindquist</span> American geneticist

Susan Lee Lindquist, ForMemRS was an American professor of biology at MIT specializing in molecular biology, particularly the protein folding problem within a family of molecules known as heat-shock proteins, and prions. Lindquist was a member and former director of the Whitehead Institute and was awarded the National Medal of Science in 2010.

Molecular evolution is the process of change in the sequence composition of cellular molecules such as DNA, RNA, and proteins across generations. The field of molecular evolution uses principles of evolutionary biology and population genetics to explain patterns in these changes. Major topics in molecular evolution concern the rates and impacts of single nucleotide changes, neutral evolution vs. natural selection, origins of new genes, the genetic nature of complex traits, the genetic basis of speciation, the evolution of development, and ways that evolutionary forces influence genomic and phenotypic changes.

Population genetics is a subfield of genetics that deals with genetic differences within and among populations, and is a part of evolutionary biology. Studies in this branch of biology examine such phenomena as adaptation, speciation, and population structure.

Gene duplication is a major mechanism through which new genetic material is generated during molecular evolution. It can be defined as any duplication of a region of DNA that contains a gene. Gene duplications can arise as products of several types of errors in DNA replication and repair machinery as well as through fortuitous capture by selfish genetic elements. Common sources of gene duplications include ectopic recombination, retrotransposition event, aneuploidy, polyploidy, and replication slippage.

<span class="mw-page-title-main">Directional selection</span> Type of genetic selection favoring one extreme phenotype

In population genetics, directional selection is a type of natural selection in which one extreme phenotype is favored over both the other extreme and moderate phenotypes. This genetic selection causes the allele frequency to shift toward the chosen extreme over time as allele ratios change from generation to generation. The advantageous extreme allele will increase as a consequence of survival and reproduction differences among the different present phenotypes in the population. The allele fluctuations as a result of directional selection can be independent of the dominance of the allele, and in some cases if the allele is recessive, it can eventually become fixed in the population.

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.

Sup35p is the Saccharomyces cerevisiae eukaryotic translation release factor. More specifically, it is the yeast eukaryotic release factor 3 (eRF3), which forms the translation termination complex with eRF1. This complex recognizes and catalyzes the release of the nascent polypeptide chain when the ribosome encounters a stop codon. While eRF1 recognizes stop codons, eRF3 facilitates the release of the polypeptide chain through GTP hydrolysis.

Genetic architecture is the underlying genetic basis of a phenotypic trait and its variational properties. Phenotypic variation for quantitative traits is, at the most basic level, the result of the segregation of alleles at quantitative trait loci (QTL). Environmental factors and other external influences can also play a role in phenotypic variation. Genetic architecture is a broad term that can be described for any given individual based on information regarding gene and allele number, the distribution of allelic and mutational effects, and patterns of pleiotropy, dominance, and epistasis.

<span class="mw-page-title-main">Pleiotropy</span> Influence of a single gene on multiple phenotypic traits

Pleiotropy occurs when one gene influences two or more seemingly unrelated phenotypic traits. Such a gene that exhibits multiple phenotypic expression is called a pleiotropic gene. Mutation in a pleiotropic gene may have an effect on several traits simultaneously, due to the gene coding for a product used by a myriad of cells or different targets that have the same signaling function.

<span class="mw-page-title-main">Facilitated variation</span>

The theory of facilitated variation demonstrates how seemingly complex biological systems can arise through a limited number of regulatory genetic changes, through the differential re-use of pre-existing developmental components. The theory was presented in 2005 by Marc W. Kirschner and John C. Gerhart.

<span class="mw-page-title-main">Canalisation (genetics)</span> Measure of the ability of a population to produce the same phenotype

Canalisation is a measure of the ability of a population to produce the same phenotype regardless of variability of its environment or genotype. It is a form of evolutionary robustness. The term was coined in 1942 by C. H. Waddington to capture the fact that "developmental reactions, as they occur in organisms submitted to natural selection...are adjusted so as to bring about one definite end-result regardless of minor variations in conditions during the course of the reaction". He used this word rather than robustness to consider that biological systems are not robust in quite the same way as, for example, engineered systems.

<span class="mw-page-title-main">Fungal prion</span> Prion that infects fungal hosts

A fungal prion is a prion that infects hosts which are fungi. Fungal prions are naturally occurring proteins that can switch between multiple, structurally distinct conformations, at least one of which is self-propagating and transmissible to other prions. This transmission of protein state represents an epigenetic phenomenon where information is encoded in the protein structure itself, instead of in nucleic acids. Several prion-forming proteins have been identified in fungi, primarily in the yeast Saccharomyces cerevisiae. These fungal prions are generally considered benign, and in some cases even confer a selectable advantage to the organism.

Genetic assimilation is a process described by Conrad H. Waddington by which a phenotype originally produced in response to an environmental condition, such as exposure to a teratogen, later becomes genetically encoded via artificial selection or natural selection. Despite superficial appearances, this does not require the (Lamarckian) inheritance of acquired characters, although epigenetic inheritance could potentially influence the result. Waddington stated that genetic assimilation overcomes the barrier to selection imposed by what he called canalization of developmental pathways; he supposed that the organism's genetics evolved to ensure that development proceeded in a certain way regardless of normal environmental variations.

<span class="mw-page-title-main">Gene redundancy</span>

Gene redundancy is the existence of multiple genes in the genome of an organism that perform the same function. Gene redundancy can result from gene duplication. Such duplication events are responsible for many sets of paralogous genes. When an individual gene in such a set is disrupted by mutation or targeted knockout, there can be little effect on phenotype as a result of gene redundancy, whereas the effect is large for the knockout of a gene with only one copy. Gene knockout is a method utilized in some studies aiming to characterize the maintenance and fitness effects functional overlap.

<span class="mw-page-title-main">Robustness (evolution)</span> Persistence of a biological trait under uncertain conditions

In evolutionary biology, robustness of a biological system is the persistence of a certain characteristic or trait in a system under perturbations or conditions of uncertainty. Robustness in development is known as canalization. According to the kind of perturbation involved, robustness can be classified as mutational, environmental, recombinational, or behavioral robustness etc. Robustness is achieved through the combination of many genetic and molecular mechanisms and can evolve by either direct or indirect selection. Several model systems have been developed to experimentally study robustness and its evolutionary consequences.

<span class="mw-page-title-main">Neofunctionalization</span>

Neofunctionalization, one of the possible outcomes of functional divergence, occurs when one gene copy, or paralog, takes on a totally new function after a gene duplication event. Neofunctionalization is an adaptive mutation process; meaning one of the gene copies must mutate to develop a function that was not present in the ancestral gene. In other words, one of the duplicates retains its original function, while the other accumulates molecular changes such that, in time, it can perform a different task.

Weak selection in evolutionary biology is when individuals with different phenotypes possess similar fitness, i.e. one phenotype is weakly preferred over the other. Weak selection, therefore, is an evolutionary theory to explain the maintenance of multiple phenotypes in a stable population.

References

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