Canalisation (genetics)

Norms of reaction for two genotypes. Genotype B shows a strongly bimodal distribution indicating differentiation into distinct phenotypes. Each phenotype is buffered against environmental variation - it is canalised.

Canalisation (canalization in American English) is a measure of the ability of a population to produce the same phenotype regardless of variability of its environment or genotype. In other words, it means robustness. The term canalisation was coined by C. H. Waddington.^[1] He used this word rather than robustness to take into account that biological systems are not robust in the quite the same way as, for example, engineered systems. Biological robustness or canalisation comes about when developmental pathways are shaped by evolution. Waddington introduced the epigenetic landscape, in which the state of an organism rolls "downhill" during development. In this metaphor, a canalised trait is illustrated as a valley enclosed by high ridges, safely guiding the phenotype to its "fate". Waddington claimed that canals form in the epigenetic landscape during evolution, and that this heuristic is useful for understanding the unique qualities of biological robustness.^[2]

Genetic assimilation

Waddington used the concept of canalisation to explain his experiments on genetic assimilation.^[3] 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 environmental induced phenotype had become inherited. Waddington explained this as the formation of a new canal in the epigenetic landscape.

It is, however, possible to explain this observation of genetic assimilation using only quantitative genetics and a threshold model, with no reference to the concept of canalisation.^[4][5][6][7] However, theoretical models that incorporate a complex genotype-phenotype map have found evidence for the evolution of phenotypic robustness^[8] contributing to genetic assimilation,^[9] even when selection is only for developmental stability and not for a particular phenotype, and so the quantitative genetics models do not apply. These studies suggest that the canalisation heuristic may still be useful, beyond the more simple concept of robustness.

Congruence hypothesis

Neither canalisation nor robustness are simple quantities to quantify: it is always necessary to specify which trait is canalised/robust to which perturbations. For example, perturbations can come either from the environment or from mutations. It has been suggested that different perturbations have congruent effects on development taking place on an epigenetic landscape.^{[10][11][12][13][14]} This could, however, depend on the molecular mechanism responsible for robustness, and be different in different cases.^[15]

Evolutionary capacitance

The canalisation metaphor suggests that phenotypes are very robust to small perturbations, for which development does not exit the canal, and rapidly returns back down, with little effect on the final outcome of development. But perturbations whose magnitude exceeds a certain threshold will break out of the canal, moving the developmental process into uncharted territory. Strong robustness up to a limit, with little robustness beyond, is a pattern that could increase evolvability in a fluctuating environment.^[16] Genetic canalization could allow for evolutionary capacitance, where genetic diversity outside the canal accumulates in a population over time, sheltered from natural selection because it does not normally affect phenotypes. This hidden diversity could then be unleashed by extreme changes in the environment or by molecular switches, releasing previously cryptic genetic variation that can then contribute to a rapid burst of evolution.

See also

• Developmental biology
• Developmental noise
• Developmental systems theory
• Evolutionary developmental biology
• Evolutionary capacitance
• Evolvability
• Gene regulatory network
• Phenotypic plasticity
• Systems biology

References

1. ^ Waddington CH (1942). "Canalization of development and the inheritance of acquired characters". Nature 150 (3811): 563–565. doi:10.1038/150563a0. 
2. ^ Waddington CH (1957). The strategy of the genes. George Allen & Unwin. 
3. ^ Waddington CH (1953). "Genetic assimilation of an acquired character". Evolution 7 (2): 118–126. doi:10.2307/2405747. JSTOR 2405747. 
4. ^ Stern C (1958). "Selection for subthreshold differences and the origin of pseudoexogenous adaptations". American Naturalist 92 (866): 313–316. doi:10.1086/282040. 
5. ^ Bateman KG (1959). "The genetic assimilation of the dumpy phenocopy". American Naturalist 56: 341–351. 
6. ^ Scharloo W (1991). "Canalization – genetic and developmental aspects". Annual Reviews in Ecology and Systematics 22: 65–93. doi:10.1146/annurev.es.22.110191.000433. 
7. ^ Falconer DS, Mackay TFC (1996). Introduction to Quantitative Genetics. pp. 309–310. 
8. ^ Siegal ML, Bergman A (2002). "Waddington's canalization revisited: Developmental stability and evolution". Proceedings of the National Academy of Sciences of the United States of America 99 (16): 10528–10532. doi:10.1073/pnas.102303999. PMC 124963. PMID 12082173. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=124963. 
9. ^ Masel J (2004). "Genetic assimilation can occur in the absence of selection for the assimilating phenotype, suggesting a role for the canalization heuristic". Journal of Evolutionary Biology 17 (5): 1106–1110. doi:10.1111/j.1420-9101.2004.00739.x. PMID 15312082. 
10. ^ Meiklejohn CD, Hartl DL (2002). "A single mode of canalization". Trends in Ecology & Evolution 17: e9035. 
11. ^ Ancel LW, Fontana W (2000). "Plasticity, evolvability, and modularity in RNA". Journal of Experimental Zoology 288 (3): 242–283. doi:10.1002/1097-010X(20001015)288:3<242::AID-JEZ5>3.0.CO;2-O. PMID 11069142. 
12. ^ Szöllősi GJ, Derényi I (2009). "Congruent Evolution of Genetic and Environmental Robustness in Micro-RNA". Molecular Biology & Evolution 26 (4): 867–874. doi:10.1093/molbev/msp008. PMID 19168567. 
13. ^ Wagner GP, Booth G Bagheri-Chaichian H (1997). "A population genetic theory of canalization". Evolution 51 (2): 329–347. doi:10.2307/2411105. JSTOR 2411105. 
14. ^ Lehner B; Lehner, Ben (2010). Polymenis, Michael. ed. "Genes Confer Similar Robustness to Environmental, Stochastic, and Genetic Perturbations in Yeast". PLoS ONE 5 (2): 468–473. doi:10.1371/journal.pone.0009035. PMC 2815791. PMID 20140261. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0009035. 
15. ^ Masel J Siegal ML (2009). "Robustness: mechanisms and consequences". Trends in Genetics 25 (9): 395–403. doi:10.1016/j.tig.2009.07.005. PMC 2770586. PMID 19717203. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2770586. 
16. ^ Eshel,I. Matessi, C. (1998). "Canalization, genetic assimilation and preadaptation: A quantitative genetic model". Genetics 4: 2119–2133.