Shifting balance theory - AbsoluteAstronomy.com

The shifting balance theory of evolution is a view of evolution advocated by Sewall Wright that each of the four evolutionary forces is important to adaptive evolution. The shifting balance theory emphasizes the roles of population subdivision and genetic drift

Genetic drift

Genetic drift or allelic drift is the change in the frequency of a gene variant in a population due to random sampling.The alleles in the offspring are a sample of those in the parents, and chance has a role in determining whether a given individual survives and reproduces...

in adaptive evolution.

Brief History

Although Sewall Wright

Sewall Wright

Sewall Green Wright was an American geneticist known for his influential work on evolutionary theory and also for his work on path analysis. With R. A. Fisher and J.B.S. Haldane, he was a founder of theoretical population genetics. He is the discoverer of the inbreeding coefficient and of...

was one of the founders of the modern evolutionary synthesis

Modern evolutionary synthesis

The modern evolutionary synthesis is a union of ideas from several biological specialties which provides a widely accepted account of evolution...

, and appreciated the power of natural selection to shape species, he had reservations about Fisher's assertion that evolutionary forces other than 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....

were of little importance to adaptive evolution.

In his early writings Wright failed to appreciate the frequency at which beneficial mutations arose (not to be confused with adaptive mutation

Adaptive mutation

Evolutionary theory describes that mutagenesis occurs randomly, regardless of the utility of a genetic mutation to the organism. If it is beneficial or neutral, the organism will survive to reproduce and pass on the mutation...

) ...

...contended that novel mutations were too infrequent and that their fixation was too slow to account for the speed of adaptive change (Wright 1931). Instead, he saw a substantial fraction of adaptations as arising by the combination of rare alleles that are deleterious by themselves, but adaptive together. Consequently, he characterized evolution as a search among these “widely separated harmonious combinations” (Wright 1932) for the best combination of alleles.

Since Wright formulated his theory it has become clear that...

...with a minimal role for mutation, is incorrect. Wright initially underestimated the contribution of novel mutation to evolution, likely owing to an influence from August Weismann

August Weismann

Friedrich Leopold August Weismann was a German evolutionary biologist. Ernst Mayr ranked him the second most notable evolutionary theorist of the 19th century, after Charles Darwin...

(?).

Empirical studies link adaptive changes in phenotypes with novel alleles arising in the recent past. For instance, pesticide resistance in Drosophila (Petrov ?). By contrast, empirical support for the importance of recombination and drift acting in concert to bring about adaptations remains weak, and because of this, the SBT has been criticized on empirical and theoretical grounds.

The Adaptive Landscape

Shortly after Wright introduced his inchoate shifting balance theory of evolution, he introduced the graphical metaphor of the adaptive landscape to help explain his theory. The adaptive landscape is a three dimensional visualization of the evolutionary process where a two dimensional surface represents all possible sequences of DNA and the third dimension represents fitness. Adjacent locations on the two dimensional surface are meant to represent similar sequences of DNA; because it is not possible to construct a graph where ... this visualization is simply metaphorical.

Hill climbing

Hill climbing

Hill climbing

In computer science, hill climbing is a mathematical optimization technique which belongs to the family of local search. It is an iterative algorithm that starts with an arbitrary solution to a problem, then attempts to find a better solution by incrementally changing a single element of the solution...

Adaptive peak

The adaptive peak is simply a fitness maximum, or high point on the fitness axis,

Adaptive Valley

the adaptive valleys are the low fitness areas between these peaks,

Adaptive Ridge

Alternatively, an adaptive ridge is a series of high fitness genotypes that connect two widely separated points in genotypic space.

Weakness of the Metaphor

Even though we get much of our terminology from this metaphor, the metaphor has limited utility because it lacks a formal mapping between genotypes and location on the surface. Therefore recombination, mutation and migration or population subdivision do not have distinct representations in the metaphor except in the simplest case of the two allele

Allele

An allele is one of two or more forms of a gene or a genetic locus . "Allel" is an abbreviation of allelomorph. Sometimes, different alleles can result in different observable phenotypic traits, such as different pigmentation...

two locus

Locus (genetics)

In the fields of genetics and genetic computation, a locus is the specific location of a gene or DNA sequence on a chromosome. A variant of the DNA sequence at a given locus is called an allele. The ordered list of loci known for a particular genome is called a genetic map...

model (Dobzhansky 1937, Elderedg 1982).

Phases

The SBT can broadly be broken into three phases:

Phase 1: Local differentiation and fitness loss: Genetic drift, disruptive selection, or gene flow create phenotypic differences between sub-populations. The equilibrium between forces may prevent populations from occupying local fitness peaks.
Phase 2: Fitness recovery: Fluctuation between the strength of all four evolutionary forces allow one or a few of these sub-populations to climb new peaks which had not previously been occupied by any substantial number of individuals.
Phase 3: Spread: Finally, these new high fitness deems then send out emigrants and the high fitness peak spreads throughout the population.

Gene flow

Mutation is a major cause of sub-population differentiation; however, mutation has been excluded as a cause of phase one because population structure does not affect the mutational process itself. In other words, mutations arise only as a function of census population numbers. The extent that population structure affects the frequency of new mutations is dependent on drift or preexisting sub-population differentiation established by drift, selection or migration.

In order for the SBT to be meaningfully different from traditional Fisharian mass selection a number of three critical criteria must be met. There must be non-additive genetic effects, a subdivided population, and gene flow.

The most fundamental of these requirements is the requirement of non-additive genetic effects. These can arise either from under-dominance or by epistatic effects on fitness. It is important to note that wright's theory depends on genetic epistasis, not epistatic variance per se (Whitlock 1995). Much as selection minimizes additive genetic variance by removing deleterious alleles from a population, selection will also minimize epistatic variance, though less efficiently. Within any given population, very little phenotypic variance might result from genetic epistasis.

A subdivided population structure is then necessary for a number of reasons. For the SBT to work, there must be some epistatic variance, however, it need not be within a single population. The epistatic variance could be masked by alternative fixation of alleles between sub-populations. Additionally, the population structure is necessary for the SBT because recombination continually removes the effect of selection on non-additive variance. It is possible for the rate of selective increase of a haplotype to exceed the rate that recombination breaks that halplotype apart, but a sub-divided population makes this transition more likely . It is important that the sub-populations have some level of gene flow, otherwise it is clear that a reduced population size will reduce the amount of variation genetic variation.

Influence of the Theory

G. G. Simpson based quantum evolution

Quantum evolution

Quantum evolution is a component of George Gaylord Simpson's multi-tempoed theory of evolutionary change, proposed to explain the rapid emergence of higher taxonomic groups. According to Simpson, evolutionary rates differ from group to group and even among closely related lineages...

on Wright's Shifting balance theory and Gould

Stephen Jay Gould

Stephen Jay Gould was an American paleontologist, evolutionary biologist, and historian of science. He was also one of the most influential and widely read writers of popular science of his generation....

and Eldredge

Niles Eldredge

Niles Eldredge is an American paleontologist, who, along with Stephen Jay Gould, proposed the theory of punctuated equilibrium in 1972.-Education:...

's punctuated equilibrium

Punctuated equilibrium

Punctuated equilibrium is a theory in evolutionary biology which proposes that most species will exhibit little net evolutionary change for most of their geological history, remaining in an extended state called stasis...

was also inspired by this theory.

Wright's Views

Wright believed that stabilizing selection could prevent the continued evolution of a species because selection would cause species to become entrapped in local fitness maxima which were substantially lower than the global maximum. As a result he believe that all four evolutionary forces were fundamentally necessary to ensure escape from these local maximum and movement to higher maxima.

"Conditions are held to be most favorable for a continuing process where there are certain states of dynamic equilibrium at many loci. This situation is found to the greatest degree in a population in which there is sufficient isolation of many local centers of population growth and emigration to provide the conditions for continual trial and error. The 'errors' are the relatively indeterminate elements in the situation: novel mutations and the effects of accidents of sampling, and of variations in the local conditions of selection and migration at the level of the local population."

However, he repeatedly denied that any one force was more responsible than any other evolutionary force for creating adaptation. The foundation of Wright's theory is the assertion that a subdivided population has greater phenotypic variability than a panmictic population, and that the phenotypic variable structured population will undergo more rapid adaptive evolution than the panmictic population. Despite Wright's protests, This definition does not involve any particular mechanism to explain the increased rate of adaptation, the specific mechanism by which moves population off of local maxima and onto new maxima; however, this does not make the theory infinity flexible and unfalsifiable.

Wright's SBT is closely associated with the metaphor of the adaptive landscape. Although Wright verbalizes his shifting balance theory (Wright 1931) before he introduces this metaphor (Wright 1932), arguably the metaphor has had the greater impact on evolutionary thought.

Wright's discusses these views in

Modern Debate

Consensus has not been reached on the importance of the Shifting Balance Process.

Empirical Studies

Perhaps the most formidable criticism of the Shifting Balance Theory is that it has little empirical support. It is important to make the distinction between empirical support for the existence of the factors which are required for the Shifting Balance Theory to operate and empirical support that the Shifting Balance Process is in fact important in nature. Non-additive genetic effects and population subdivision are necessary for Wright's Shifting Balance Theory, but demonstrating their existence is insufficient to establish the general importance of the Shifting Balance Theory.

Molecular Genetics

Evidence of epistasis may not be apparent from intrapopulation comparisons of segregating variation, because alleles are co-evolved and much negative epistasis can be removed by selection.

Quantitative Genetics

However, inter-population comparisons commonly demonstrate F1 heterosis

Heterosis

Heterosis, or hybrid vigor, or outbreeding enhancement, is the improved or increased function of any biological quality in a hybrid offspring. The adjective derived from heterosis is heterotic....

and F2 hybrid brake down. Heterosis is almost certainly due to under-dominance at many of the loci in the F1 generation. It is interesting to note that heterosis is commonly observed in plants, where there has been few loci have been characterized as being under balancing selection. The F2 generation has similar levels of heterozygousity as the F1 generation, so the commonly observed depression of fitness relative to the substantially more homozygous P generation supports the idea that gene complexes are common co-evolved or co-adapted, and that recombination can break these complexes up, leading to a depression in fitness. Although there are some excellent examples where the interaction of factors that create epistasis for fitness is well understood, such as the interaction of cryptic coloration and anti-predator behavior in snakes (Brodie 1992), typically the nature of the epistasis leading to F2 hybrid breakdown is unknown. It is possible that Dobzhansky-Muller incompatibility cause this breakdown, so F2 hybrid break down is not sufficient evidence that a fitness valley has been crossed.
A final piece of evidence is relevant to the of epistasis: Out-breeding depression seems to involve few loci, implying that moving between alternative peaks can be accomplished with a small number of adaptations (Edmans et al. 2005). The SBT need not operate at every locus to be evolutionarily important. Once a peak shift has occurred at a single locus due to the SBT, a cascade of fixations may occur by fisherian mass-selection. Clearly a single allelic substation can initiate these cascades, as in that case of the pollinator shift between Mimulus lewisii and M. cardinalis (Bradshaw and Schemske 2003).

Complex adaptation

If it can be shown that populations do in fact experience short periods of low fitness and lowered populations before novel adaptations arise, this would be important evidence supporting the shifting balance theory.

There are two routes to fix a complex adaptation which has deleterious intermediates: sequential fixation vs. stochastic tunneling. In the case of sequential fixation, a population most first fix an allele which is deleterious; however, a population may also fix an adaptive mutation without the deleterious intermediate ever rising above selection-mutation equilibrium by a process called stochastic tunneling (Lynch and Abegg 2010). This occurs because very large populations may maintain a large absolute number of deleterious alleles despite their small relative frequency.
In general sequential fixation proceeds faster in small populations, where drift is strongest, and stochastic tunneling proceeds faster in large populations. The rate of sequential fixation is not as strongly influenced by the complexity of a mutation as the rate of stochastic tunneling, and as a result if an adaptation is sufficiently complex, populations may be forced to transverse fitness valleys. (Lynch and Abegg 2010, Weismann et al. 2010). Stochastic tunneling is fundamentally different from Fisharian mass-selection, and may reflect patterns more typical of the SBT. For instance, it is unclear how population subdivision affects the time to establishment of complex mutations. If population subdivision generally increase the mean mutation load of a large population, then it will likely increase the rate of stochastic tunnelling, and this result would be very similar to predictions of Wright's shifting balance theory.

Furthermore, studies of correlated evolution in protein residues provide compelling evidence that complex adaptations are ubiquitous throughout the genome (Callahan et al. 2011, Ridout, Dixon and Filatov 2010 ). These two studies both found that amino acid substitution tended to cluster in proteins and within lineages. In particular, Callahan et al. convincingly argue that greater than 7% of protein substitutions compensate for local disruptions to protein charge. Much of the pattern found in these studies can be explained by proteins shifting between equally stable states by drift.

Wright's verbal theory is joined with a geometric metaphor. This metaphor is appealing because it allows us to visualize the action of evolution as a hill climbing phenomenon, which is easily understood (Coyne, B and T 1997). The pedagogical utility of the metaphor may have led to a wider awareness of the shifting balance theory that it described than would have occurred otherwise. Additionally there is an element of historical contingency: the shifting balance theory was proposed by an influential author and discussed by other influential authors during the formation of the modern synthesis (Elderage 1987). Wright's theory postulates a role for each of the evolutionary forces in producing adaptation, which makes Fisharian mass-selection seem like a special case of the more general shifting balance theory. The complex mathematics involved, appealing pedagogical metaphor, central place in during the formation of the modern synthesis and the difficulty of empirically evaluating the theory all help ensure the protracted interest in this theory.