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."^[1] This usage is unrelated to the usage below.

Genetic assimilation is a process 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 inheritance of acquired characters, although epigenetic inheritance could potentially influence the result.^[2] Genetic assimilation is merely a method of overcoming the barrier to selection imposed by genetic canalization of developmental pathways.

If there is no canalization of a developmental pathway, genetic variation of pathway components results in a continuous spectrum of phenotypes, often distributed in a bell curve. In these cases artificial selection can be done in a straightforward way, by choosing offspring from one end of the curve and using them to breed the next generation. However, when a pathway is strongly canalized, all of the individuals, except perhaps a few at the furthest extreme of the bell curve, physically look the same regardless of their genotype under normal environmental circumstances. However, a given genetic make-up does not predetermine the same outcome under all possible circumstances; instead, it determines a norm of reaction that varies with the environment (phenotypic plasticity). There may be a way to stress an organism so that canalization breaks down, and many aberrant individuals can be selected for further breeding; these are said to phenocopy the desired genetic trait. With several generations of artificial selection in this manner, perhaps aided by mutagenesis, the genetic variation can be reduced to that of the furthest extreme of the original population, until canalization is overwhelmed even under normal environmental conditions. At this point the environmentally induced abnormality has been duplicated genetically.

The classic example of genetic assimilation was a 1953 experiment by C. H. Waddington, in which Drosophila fruit fly embryos were exposed to ether, producing a bithorax-like phenotype^[3] (a homeotic change). Flies which developed halteres with wing-like characteristics were chosen for breeding for 20 generations, by which point the phenotype could be seen without ether treatment.

Genetic assimilation in natural selection

It has not been proven that genetic assimilation occurs in natural evolution, but it is difficult to rule it out from having at least a minor role, and research continues into the question.^[4] Mathematical modeling suggests that under certain circumstances, natural selection will favor the evolution of canalization that is designed to fail under extreme conditions.^[5] If the result of such a failure is favored by natural selection, genetic assimilation will occur. In the 1960s C. H. Waddington and J. M. Rendel argued for the importance of genetic assimilation in natural adaptation as a means of providing new and potentially beneficial variation to populations under stress. Their contemporary Williams argued that genetic assimilation proceeds at the cost of a loss of developmental plasticity, and should be a minor mechanism. If it occurs frequently, genetic assimilation could contribute to punctuated equilibrium in evolution, as organisms repeatedly evolve systems of canalization, then break out of them under adverse circumstances.

Waddington's experiment

To illustrate the phenomenon, Waddington (1942) managed to induce an extreme environmental reaction in the developing embryos of Drosophila.^[6] In response to ether vapor a proportion of embryos developed a radical phenotypic change, a second thorax. At this point in the experiment we would say that bithorax isn't innate; it is a kind of chimera induced by an unusual environment. But then Waddington continually selected for Drosophila with the developmental capacity to respond to the environmental stress. After about 20 generations of selection, some Drosophila were obtained that developed bithorax without being exposed to ether treatment. What happened, according to Waddington, is that selection favored a particular pathway that led to the production of the optimal (in this case desired) effect. Eventually the pathway became canalized, hence the end-state, bithorax, appeared regardless of environmental conditions.^[6]

Another version: Waddington used the concept of canalisation to explain his experiments on genetic assimilation. In these experiments, he exposed Drosophila pupae to heat shock. This environmental disturbance caused some flies to develop a crossveinless phenotype. He then selected for crossveinless. Eventually, the crossveinless phenotype appeared even without heat shock. Through this process of genetic assimilation, an environmentally induced phenotype had become inherited. Waddington explained this as the formation of a new canal in the epigenetic landscape.

Neo-Darwinism or Lamarckism?

Waddington's theory of genetic assimilation was controversial.^[7][8] The evolutionary biologists Theodosius Dobzhansky and Ernst Mayr both thought that Waddington was using genetic assimilation to support so-called Lamarckian inheritance. They denied that the inheritance of acquired characteristics had taken place, and asserted that Waddington had simply observed the natural selection of genetic variants that already existed in the study population.^[9] Waddington himself interpreted his results in a Neo-Darwinian way, particularly emphasizing that they "could bring little comfort to those who wish to believe that environmental influences tend to produce heritable changes in the direction of adaptation."^[2][10]

The conventional evolutionary view of genetic assimilation is that a trait is expressed when the quantitatve values of alleles favoring it exceed a threshold. Waddington's perturbations decrease the value of this threshold, facilitating natural selection for the trait and its underlying alleles, increasing the frequency of those alleles to the point where the trait is expressed even in the absence of the perturbation.^[11]

Adam S. Wilkins wrote that "[Waddington] in his lifetime... was widely perceived primarily as a critic of Neo-Darwinian evolutionary theory. His criticisms ... were focused on what he saw as unrealistic, 'atomistic' models of both gene selection and trait evolution." In particular, according to Wilkins, Waddington felt that the Neo-Darwinians badly neglected the phenomenon of extensive gene interactions and that the 'randomness' of mutational effects, posited in the theory, was false.^[12] Even though Waddington became critical of the neo-Darwinian synthetic theory of evolution, he still described himself as a Darwinian, and called for an extended evolutionary synthesis based on his research.^[12][13] Waddington did not deny the threshold-based conventional genetic interpretation of his experiments, but regarded it "as a "told to the children" version of what I wished to say" and considered the debate to be about "mode of expression, rather than of substance".^[14]

Reviewing the debate in 2015, the systems biologist Denis Noble writes that

[Waddington] did not describe himself as a Lamarckian, but by revealing mechanisms of inheritance of acquired characteristics, I think he should be regarded as such. The reason he did not do so is that Lamarck could not have conceived of the processes that Waddington revealed. Incidentally, it is also true to say that Lamarck did not invent the idea of the inheritance of acquired characteristics. But, whether historically correct or not, we are stuck today with the term 'Lamarckian' for inheritance of a characteristic acquired through an environmental influence.^[15]

Related concepts

Genetic assimilation generally describes the production of phenotypes with altered or decreased responsiveness to environmental conditions; the phenotype produced under a stressful condition becomes the phenotype for every condition.^[2] Genetic accommodation can be used to refer more broadly to changes in gene frequency that result from environmentally induced phenotypes. When used by contrast with genetic assimilation, the term can be applied more specifically to refer to the outcome that may be obtained when selection under stressful conditions is used to obtain a phenotype with increased responsiveness to environmental conditions. For example, Y. Suzuki and H.F. Nijhout found that a black mutant line of Manduca sexta caterpillars sometimes became green under heat-shock conditions; selection of green caterpillars for thirteen generations yielded a polyphenic line that reliably became green under heat-shock, but remained black at cool temperatures.^[16] Either genetic assimilation or (other) genetic accommodation can be produced by similar selection procedures, and it may not be possible to predict in advance which phenomenon will occur. The underlying biological basis of these phenomena can be quite similar — temperature sensitive mutations and mutations affecting the activity of a gene without temperature sensitivity can each be produced by a small change in the sequence of a protein.

Genetic compensation describes the situation that occurs when an environmental condition changes the phenotype, but the new phenotype is not favored by selection. The outcome is a genetic change that shifts the expressed phenotype back to its original state despite the altered environment. For example, in salmon, anadromous sockeye populations migrate into the ocean to develop, where they ingest high levels of carotenoids which they use to produce an intense red coloration. "Residuals", salmon which do not enter the ocean, do not receive this nutrition and are a green color. However, they are thought to be the progenitors of nonanadromous kokanee salmon, which despite remaining in freshwater lakes develop an intense red coloration. Similar situations can be described for the pigmentation of tanagers and guppies. Genetic compensation may play a role in speciation by creating genetic incompatibilities between phenotypically similar populations within a species.^[17]

Genetic assimilation experiments have been comparatively rare in modern studies, because most geneticists are more interested in relating the activity of a gene to that of other genes. Those relationships are pursued by the study of genetic interaction, which is similar in concept. In a genetic interaction study, the experimenter begins with a strain that has a weak phenotype due to a known mutant allele, and screens flies for second mutations that create a stronger phenotype. Genetic interaction studies are typically used to identify mutant alleles with relatively severe effects, at least in the genetic background of the known mutant allele, which can be readily localized by genetic mapping and further characterized. The objective of these studies is to work out which genes have related functions --- often genes paired in this manner are later shown to code proteins that physically interact within the cell or catalyze sequential steps of a chemical reaction.

Current status

There has been a reignited interest in genetic assimilation as scientists have identified a molecular basis for Waddington's observations.^[18] A group of scientists have also discovered evidence for genetic assimilation due to the evolution of the large heads of tiger snakes.^[19]

Waddington's work on genetic assimilation (GA) has been merged into the extended evolutionary synthesis. On the subject (Massimo Pigliucci et al. 2006) have written "concepts such as GA and phenotypic accommodation, represent not a threat to the modern synthesis, but rather a welcome expansion of its current horizon."^[8]

See also

• Canalisation (genetics)
• Evolutionary developmental biology
• List of genetics-related topics

References

Further reading

• Crispo, Erika. (2007). "The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity". Evolution 61: 2469-2479.