Evolvability
Encyclopedia
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 to evolve by natural selection, there must be a certain minimum probability that new, heritable variants are beneficial. Random mutations, unless they occur in DNA sequences with no function, are expected to be mostly detrimental. Beneficial mutations are always rare, but if they are too rare, then adaptation
cannot occur. Early failed efforts to evolve computer programs by random mutation and selection showed that evolvability is not a given, but depends on the representation of the program. Analogously, the evolvability of organisms depends on their genotype-phenotype map. This means that biological genomes are structured in ways that make beneficial changes less unlikely than they would otherwise be. This has been taken as evidence that evolution has created not just fitter organisms, but populations of organisms that are better able to evolve.
According to the second definition, a biological system is evolvable
For example, consider an enzyme
with multiple alleles in the population. Each allele catalyzes the same reaction, but with a different level of activity. However, even after millions of years of evolution, exploring many sequences with similar function, no mutation might exist that gives this enzyme the ability to catalyze a different reaction. Thus, although the enzyme’s activity is evolvable in the first sense, that does not mean that the enzyme's function is evolvable in the second sense. However, every system evolvable in the second sense must also be evolvable in the first.
Pigliucci recognizes three classes of definition, depending on timescale. The first corresponds to Wagner's first, and represents the very short timescales that are described by quantitative genetics
. He divides Wagner's second definition into two categories, one representing the intermediate timescales that can be studied using population genetics
, and one representing exceedingly rare long-term innovations of form.
Altenberg introduced a quantitative concept of Pigliucci's second evolvability definition, being not a single number, but the entire upper tail of the fitness distribution of the offspring produced by the population. This quantity was considered a "local" property of the instantaneous state of a population, and its integration over the population's evolutionary trajectory, and over many possible populations, would be necessary to give a more global measure of evolvability.
will not increase evolvability in the first sense. In organisms with a high level of robustness, mutations will have smaller phenotypic effects than in organisms with a low level of robustness. Thus, robustness reduces the amount of heritable genetic variation on which selection can act. However, robustness may allow exploration of large regions of genotype space, increasing robustness according to the second sense.
For example, one reason many proteins are less robust to mutation is that they have marginal thermodynamic stability
, and most mutations reduce this stability further. Proteins that are more thermostable can tolerate a wider range of mutations, and are more evolvable.
Functional variation in a population may be unfavorable in a constant environment, but useful in a changing one. Robust or degenerate ensembles
can appear functionally redundant in certain environmental contexts but functionally diverse in others. In other words, in a genetically robust system, cryptic genetic variation will accumulate. Because degeneracy allows for genetic exploration under conditions that require the selective retention of functions/traits, it has been hypothesized to increase evolvability.
exists, many mutants will persist in a cryptic state. Mutations tend to fall into two categories, having either a very bad effect or very little effect: few mutations fall somewhere in between. Sometimes, these mutations will not be completely invisible, but still have rare effects, with very low penetrance
. When this happens, natural selection weeds out the really bad mutations, while leaving the other mutations relatively unaffected. While evolution has no "foresight" to know which environment will be encountered in the future, some mutations cause major disruption to a basic biological process, and will never be adaptive in any environment. Screening these out in advance leads to preadapted
stocks of cryptic genetic variation.
Another way that phenotypes can be explored, prior to strong genetic commitment, is through learning. An organism that learns gets to "sample" several different phenotypes during its early development, and later sticks to whatever worked best. Later in evolution, the optimal phenotype can be genetically assimilated
so it becomes the default behavior rather than a rare behavior. This is known as the Baldwin effect
, and it can increase evolvability.
Learning biases phenotypes in a beneficial direction. But an exploratory flattening of the fitness landscape
can also increase evolvability even when it has no direction, for example when the flattening is a result of random errors in molecular and/or developmental processes. This increase in evolvability can happen when evolution is faced with crossing a "valley" in an adaptive landscape
. This means that two mutations exist that are deleterious by themselves, but beneficial in combination. These combinations can evolve more easily when the landscape is first flattened, and the discovered phenotype is then fixed by genetic assimilation
.
is restricted to within functional modules
, then mutations affect only one trait at a time, and adaptation is much easier.
via a mutator allele would increase evolvability. But as an extreme example, if the mutation rate is too high then all individuals will be dead or at least carry a heavy mutation load
. Short-term selection for low variation most of the time is usually thought likely to be more powerful than long-term selection for evolvability, making it difficult for natural selection to cause the evolution of evolvability.
When recombination is low, mutator alleles may still sometimes hitchhike
on the success of adaptive mutations that they cause. In this case, selection can take place at the level of the lineage. This may explain why mutators are often seen during experimental evolution
of microbes. Mutator alleles can also evolve more easily when they only increase mutation rates in nearby DNA sequences, not across the whole genome: this is known as a contingency locus.
The evolution of evolvability is less controversial if it occurs via the evolution of sexual reproduction, or via the tendency of variation-generating mechanisms to become more active when an organism is stressed. The yeast prion
[PSI+] may also be an example of the evolution of evolvability through evolutionary capacitance
. An evolutionary capacitor is a switch that turns genetic variation on and off. This is very much like bet-hedging the risk that a future environment will be similar or different. Theoretical models also predict the evolution of evolvability via modularity. When the costs of evolvability are sufficiently short-lived, more evolvable lineages may be the most successful in the long-term.
Evolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
. Evolvability is the ability of a population of organisms to not merely generate genetic diversity
Genetic diversity
Genetic diversity, the level of biodiversity, refers to the total number of genetic characteristics in the genetic makeup of a species. It is distinguished from genetic variability, which describes the tendency of genetic characteristics to vary....
, but to generate adaptive
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....
genetic diversity, and thereby evolve through 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....
.
In order for a biological organism to evolve by natural selection, there must be a certain minimum probability that new, heritable variants are beneficial. Random mutations, unless they occur in DNA sequences with no function, are expected to be mostly detrimental. Beneficial mutations are always rare, but if they are too rare, then 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....
cannot occur. Early failed efforts to evolve computer programs by random mutation and selection showed that evolvability is not a given, but depends on the representation of the program. Analogously, the evolvability of organisms depends on their genotype-phenotype map. This means that biological genomes are structured in ways that make beneficial changes less unlikely than they would otherwise be. This has been taken as evidence that evolution has created not just fitter organisms, but populations of organisms that are better able to evolve.
Alternative definitions
Wagner describes two definitions of evolvability. According to the first definition, a biological system is evolvable- if its properties show heritable genetic variation, and
- if natural selection can thus change these properties.
According to the second definition, a biological system is evolvable
- if it can acquire novel functions through genetic change, functions that help the organism survive and reproduce.
For example, consider an enzyme
Enzyme
Enzymes are proteins that catalyze chemical reactions. In enzymatic reactions, the molecules at the beginning of the process, called substrates, are converted into different molecules, called products. Almost all chemical reactions in a biological cell need enzymes in order to occur at rates...
with multiple alleles in the population. Each allele catalyzes the same reaction, but with a different level of activity. However, even after millions of years of evolution, exploring many sequences with similar function, no mutation might exist that gives this enzyme the ability to catalyze a different reaction. Thus, although the enzyme’s activity is evolvable in the first sense, that does not mean that the enzyme's function is evolvable in the second sense. However, every system evolvable in the second sense must also be evolvable in the first.
Pigliucci recognizes three classes of definition, depending on timescale. The first corresponds to Wagner's first, and represents the very short timescales that are described by quantitative genetics
Quantitative genetics
Quantitative genetics is the study of continuous traits and their underlying mechanisms. It is effectively an extension of simple Mendelian inheritance in that the combined effects of one or more genes and the environments in which they are expressed give rise to continuous distributions of...
. He divides Wagner's second definition into two categories, one representing the intermediate timescales that can be studied using population genetics
Population genetics
Population genetics is the study of allele frequency distribution and change under the influence of the four main evolutionary processes: natural selection, genetic drift, mutation and gene flow. It also takes into account the factors of recombination, population subdivision and population...
, and one representing exceedingly rare long-term innovations of form.
Altenberg introduced a quantitative concept of Pigliucci's second evolvability definition, being not a single number, but the entire upper tail of the fitness distribution of the offspring produced by the population. This quantity was considered a "local" property of the instantaneous state of a population, and its integration over the population's evolutionary trajectory, and over many possible populations, would be necessary to give a more global measure of evolvability.
Generating more variation
More heritable phenotypic variation means more evolvability. While mutation is the ultimate source of heritable variation, its permutations and combinations also make a big difference. Sexual reproduction generates more variation (and thereby evolvability) relative to asexual reproduction (see evolution of sexual reproduction). Evolvability is further increased by generating more variation when an organism is stressed, and thus likely to be less well adapted, but less variation when an organism is doing well. The amount of variation generated can be adjusted in many different ways, for example via the mutation rate, via the probability of sexual vs. asexual reproduction, via the probability of outcrossing vs. inbreeding, and via dispersal.Enhancement of Selection
Rather than creating more phenotypic variation, some mechanisms increase the intensity and effectiveness with which selection acts on existing phenotypic variation. For example:- Mating rituals that allow sexual selectionSexual selectionSexual selection, a concept introduced by Charles Darwin in his 1859 book On the Origin of Species, is a significant element of his theory of natural selection...
on "good genes", and so intensify natural selectionNatural selectionNatural 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.... - Large population size
- Recombination decreasing the importance of the Hill-Robertson effectHill-Robertson effectThe Hill-Robertson effect is a population genetics phenomenon first identified by Bill Hill and Alan Robertson in 1966. It describes an evolutionary advantage to genetic recombination.-Explanation:...
, where different genotypes contain different adaptive mutations. Recombination brings the two alleles together, creating a super-genotype in place of two competing lineages. - Shorter generation time
Robustness and evolvability
RobustnessMutational 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...
will not increase evolvability in the first sense. In organisms with a high level of robustness, mutations will have smaller phenotypic effects than in organisms with a low level of robustness. Thus, robustness reduces the amount of heritable genetic variation on which selection can act. However, robustness may allow exploration of large regions of genotype space, increasing robustness according to the second sense.
For example, one reason many proteins are less robust to mutation is that they have marginal thermodynamic stability
Protein 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....
, and most mutations reduce this stability further. Proteins that are more thermostable can tolerate a wider range of mutations, and are more evolvable.
Functional variation in a population may be unfavorable in a constant environment, but useful in a changing one. Robust or degenerate ensembles
Degeneracy (biology)
Within biological systems, degeneracy refers to circumstances where structurally dissimilar components/modules/pathways can perform similar functions under certain conditions, but perform distinct functions in other conditions. Degeneracy is thus a relational property that requires comparing the...
can appear functionally redundant in certain environmental contexts but functionally diverse in others. In other words, in a genetically robust system, cryptic genetic variation will accumulate. Because degeneracy allows for genetic exploration under conditions that require the selective retention of functions/traits, it has been hypothesized to increase evolvability.
Exploration ahead of time
When mutational robustnessMutational 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...
exists, many mutants will persist in a cryptic state. Mutations tend to fall into two categories, having either a very bad effect or very little effect: few mutations fall somewhere in between. Sometimes, these mutations will not be completely invisible, but still have rare effects, with very low penetrance
Penetrance
Penetrance in genetics is the proportion of individuals carrying a particular variant of a gene that also express an associated trait . In medical genetics, the penetrance of a disease-causing mutation is the proportion of individuals with the mutation who exhibit clinical symptoms...
. When this happens, natural selection weeds out the really bad mutations, while leaving the other mutations relatively unaffected. While evolution has no "foresight" to know which environment will be encountered in the future, some mutations cause major disruption to a basic biological process, and will never be adaptive in any environment. Screening these out in advance leads to preadapted
Preadaptation
In evolutionary biology, preadaptation describes a situation where a species evolves to use a preexisting structure or trait inherited from an ancestor for a potentially unrelated function...
stocks of cryptic genetic variation.
Another way that phenotypes can be explored, prior to strong genetic commitment, is through learning. An organism that learns gets to "sample" several different phenotypes during its early development, and later sticks to whatever worked best. Later in evolution, the optimal phenotype can be genetically assimilated
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....
so it becomes the default behavior rather than a rare behavior. This is known as the Baldwin effect
Baldwin effect
The Baldwin effect, also known as Baldwinian evolution or ontogenic evolution, is a theory of a possible evolutionary processes that was originally put forward in 1896 in a paper, "A New Factor in Evolution," by American psychologist James Mark Baldwin. The paper proposed a mechanism for specific...
, and it can increase evolvability.
Learning biases phenotypes in a beneficial direction. But an exploratory flattening of 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...
can also increase evolvability even when it has no direction, for example when the flattening is a result of random errors in molecular and/or developmental processes. This increase in evolvability can happen when evolution is faced with crossing a "valley" in an adaptive 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...
. This means that two mutations exist that are deleterious by themselves, but beneficial in combination. These combinations can evolve more easily when the landscape is first flattened, and the discovered phenotype is then 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....
.
Modularity
If every mutation affected every trait, then a mutation that was an improvement for one trait would be a disadvantage for other traits. This means that almost no mutations would be beneficial overall. But if pleiotropyPleiotropy
Pleiotropy occurs when one gene influences multiple phenotypic traits. Consequently, a mutation in a pleiotropic gene may have an effect on some or all traits simultaneously...
is restricted to within functional modules
Modularity
Modularity is a general systems concept, typically defined as a continuum describing the degree to which a system’s components may be separated and recombined. It refers to both the tightness of coupling between components, and the degree to which the “rules” of the system architecture enable the...
, then mutations affect only one trait at a time, and adaptation is much easier.
Evolution of evolvability
While variation yielding high evolvability could be useful in the long term, in the short term most of that variation is likely to be a disadvantage. For example, naively it would seem that increasing the mutation rateMutation rate
In genetics, the mutation rate is the chance of a mutation occurring in an organism or gene in each generation...
via a mutator allele would increase evolvability. But as an extreme example, if the mutation rate is too high then all individuals will be dead or at least carry a heavy mutation load
Genetic load
In population genetics, genetic load or genetic burden is a measure of the cost of lost alleles due to selection or mutation...
. Short-term selection for low variation most of the time is usually thought likely to be more powerful than long-term selection for evolvability, making it difficult for natural selection to cause the evolution of evolvability.
When recombination is low, mutator alleles may still sometimes hitchhike
Genetic hitchhiking
Genetic hitchhiking is the process by which an allele may increase in frequency by virtue of being linked to a gene that is positively selected. Proximity on a chromosome may allow genes to be dragged along with a selective sweep experienced by an advantageous gene nearby...
on the success of adaptive mutations that they cause. In this case, selection can take place at the level of the lineage. This may explain why mutators are often seen during experimental evolution
Experimental evolution
In evolutionary and experimental biology, the field of experimental evolution is concerned with testing hypotheses and theories of evolution by use of controlled experiments. Evolution may be observed in the laboratory as populations adapt to new environmental conditions and/or change by such...
of microbes. Mutator alleles can also evolve more easily when they only increase mutation rates in nearby DNA sequences, not across the whole genome: this is known as a contingency locus.
The evolution of evolvability is less controversial if it occurs via the evolution of sexual reproduction, or via the tendency of variation-generating mechanisms to become more active when an organism is stressed. The yeast 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...
[PSI+] may also be an example of the evolution of evolvability through evolutionary capacitance
Evolutionary capacitance
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...
. An evolutionary capacitor is a switch that turns genetic variation on and off. This is very much like bet-hedging the risk that a future environment will be similar or different. Theoretical models also predict the evolution of evolvability via modularity. When the costs of evolvability are sufficiently short-lived, more evolvable lineages may be the most successful in the long-term.