Mutationism

Mutationism (sometimes, “Mendelism”) refers to the theory emphasizing mutation as a creative principle and source of discontinuity in evolutionary change, particularly associated with the founders of modern genetics.

The discovery of genetics challenges Darwin's theory

As the 20th century dawned, geneticists learned that discontinuous variations could arise by mutation and be transmitted to offspring via stable non-mixing factors: the rules of transmission of these factors constitute Mendel’s laws. A more revolutionary discovery, from the perspective of evolutionary theory, was that slight variations in quantitative traits that emerge reliably every generation— like the "fluctuations" on which Charles Darwin built his theory— were not heritable. This result was shown in a series of breeding experiments carried out by the Danish biologist Wilhelm Johannsen. From mixtures of different true-breeding varieties of beans of different sizes, selection on a breeding population could be used to sort out the large from the small varieties, but would not change their heights, even though fluctuations in size continued to appear each generation, following the familiar normal distribution.

This result was understood widely as a direct threat to the "Natural Selection" theory of Darwin, who argued in The Origin of Species ^[1] that

"Natural selection can act only by the preservation and accumulation of infinitesimally small inherited modifications, each profitable to the preserved being; and as modern geology has almost banished such views as the excavation of a great valley by a single diluvial wave, so will natural selection, if it be a true principle, banish the belief of the continued creation of new organic beings, or of any great and sudden modification in their structure." (Ch. 4, OOS)

Darwin knew that discontinuous variations or "sports" occurred, and that their effects were heritable, but he argued that such changes would not be important in evolution, which must occur gradually according to the doctrine of natura non facit salta (see gradualism). In Darwin's theory, infinitesimal hereditary variation arises automatically in response to the effect of "altered conditions of life" on "the sexual organs"; whenever conditions change, adaptation happens automatically (and by infinitesimal increments) as selection preserves fluctuations that fit the new conditions. That is, Darwin proposed a mechanism of automatic evolution, based on automatic variation that would always be present when needed.

However, genetics showed that the kind of variation that arises automatically in response to altered conditions is not genetic variation, but non-heritable environmental variation. Heritable variation, by contrast, arises spontaneously by events of "mutation". This is how the discovery of genetics forced a re-appraisal of the mechanism of evolution — a re-appraisal that led to the rise of "mutationism".

Mutationism

Though later associated with Mendelian genetics, mutationism began in the 1890s (prior to the rediscovery of Mendel’s laws) with the studies of Hugo De Vries ^[2] and William Bateson ^[3] on naturally occurring discontinuous variations; their thoughts concerning the role of discontinuity in evolution drew on earlier ideas of William Keith Brooks, Francis Galton, and Thomas Henry Huxley.

The "mutationist" view began by abandoning Darwin's idea of automatic fluctuation, embracing instead the concept that variation emerges by rare events of mutations. This view was expressed in the writings of key founders of genetics, including Thomas Hunt Morgan, Reginald Punnett, Wilhelm Johannsen, Hugo de Vries, William Bateson and others. Assuming that heritable variation cannot be taken for granted, the mutationists saw evolution as a two-step process of the chance occurrence of a mutation, followed by its persistence or elimination (selection). The mutationists denied that selection is creative, and they gave mutation a certain measure of control over the course of evolution.^[4]

A common misconception is that the mutationists denied selection. Instead, mutationists such as Morgan simply understood its role differently. In the following passage, Morgan (writing in 1916 ^[5]) displays a clear understanding of the concept of the probability of fixation of a new mutation, which might be deleterious, neutral, or advantageous:

"If through a mutation a character appears that is neither advantageous nor disadvantageous, but indifferent, the chance that it may become established in the race is extremely small, although by good luck such a thing may occur rarely. It makes no difference whether the character in question is a dominant or a recessive one, the chance of its becoming established is exactly the same. If through a mutation a character appears that has an injurious effect, however slight this may be, it has practically no chance of becoming established. If through a mutation a character appears that has a beneficial influence on the individual, the chance that the individual will survive is increased, not only for itself, but for all of its descendants that come to inherit this character. It is this increase in the number of individuals possessing a particular character, that might have an influence on the course of evolution."

Morgan resisted calling this process "Natural Selection" because it differed so much from Darwin's view.

Demise of Mutationism and Rise of the Modern Synthesis

While the mutationist view was very popular in the first 3 decades of the 20th century, it was replaced eventually by the Darwinian view expressed in the Modern Synthesis. In 1902 G. Udny Yule argued that a trait reflecting effects of multiple Mendelian characters could show a normal distribution. Thus, even though variations that arise in response to altered conditions are environmental and non-heritable (contrary to Darwin's assumptions), some of the continuous variation in natural species could have a genetic basis, and could serve as the Mendelian basis for Darwinian gradualism. Nevertheless, the synthesis of Mendelian genetics and Darwinism later put forth by R. A. Fisher and others did not develop immediately, for various reasons: it could be doubted that natural selection was sufficiently powerful to act on infinitesimal differences; it could be doubted that natural populations had enough heritable variation to support a Darwinian view; a common (erroneous) belief at the time (following Francis Galton's notion of regression to the mean) held that even heritable fluctuations could not lead to large or qualitative changes; and some advocates of Darwinism, such as Karl Pearson, refused to accept Mendelian genetics. A key conceptual innovation of the Modern Synthesis, crucial for its acceptance,^[4] was the "gene pool" concept, which argued that natural populations "maintain" abundant heritable variation through a combination of recombination, mixis, recessivity, heterosis and balancing selection.

At the time of the Darwin centennial in Cambridge in 1909, Mutationism and Lamarckism were contrasted with Darwin's “Natural Selection” as competing ideas; 50 years later, at the University of Chicago centennial ^[6] of the publication of The Origin of Species, mutationism (like Lamarckism) was no longer seriously considered.

Nevertheless, after another 50 years, evolutionary biologists are re-considering the mutationist view.

Contemporary status of mutationism

With the arrival of molecular biology, scientists studying "molecular evolution" began to suggest mutational explanations for patterns such as genomic nucleotide composition,^[7] and eventually it became a characteristic of the field of molecular evolution to emphasize the role of mutation in evolution. ^[8] Contemporary interest in mutationism is revealed by articles in mainstream research journals that advocate mutationist ideas, referring to Goldschmidt's concept of the Hopeful Monster,^[9] or using the label "mutationism" ^[4] or "neo-mutationism".^[10][11] Phrases such as "new mutations" or "mutation-driven evolution" also indicate a departure from the "shifting gene frequencies" view of the Modern Synthesis, in which evolution consists of establishing a new multi-locus equilibrium for the frequencies of pre-existing alleles, without new mutations.^[4]

These contemporary writings suggest that mutation plays a role in evolution that was proposed by the "mutationists" but rejected in the Modern Synthesis. A key aspect of this role, advocated forcefully in mainstream journals, is "how single mutations can have huge effects that drive evolution",^[9] a result that is difficult to argue from retrospective analyses, but that appears clearly in laboratory evolution experiments, such as those of Lenski and colleagues (cited in ^[9]). According to Takahata,^[12]

"Unlike neo-Darwinism, which regards mutation as merely raw material and natural selection as the creative power, Nei's mutationism assumes that the most fundamental process for adaptive evolution is the production of functionally more efficient genotypes by mutation (especially birth and death of duplicated genes) and by recombination."

Another aspect of this role, discussion of which is restricted largely to trade journals in molecular evolution and genomics, is that patterns of diversity and rates of change reflect systematic biases in mutation.^[13] Stoltzfus and Yampolsky ^[4][13][14] list examples in which mutation-biased evolution is either a plausible hypothesis or the received view. A case that has received much attention is in regard to genomic GC-content and the origin of isochore.^[15] The mutational hypothesis is that systematic differences in GC content emerge slowly due to the cumulative effect of mutational biases favoring GC or AT.^[16][17][18] However, because the bond is stronger and more resilient between the G:C pairs than between A:T pairs, a commonly proposed selective explanation is that a high GC-content is an adaption to harsh conditions, either high temperature ^[19] or UV radiation.^[20] Both hypotheses were later disproved.^[21][22]

See also

• Molecular evolution
• History of evolutionary thought
• History of molecular evolution

References

1. ^ Darwin, C (1859). On the Origin of Species. 
2. ^ De Vries, H (1905). Species and Varieties: their Origin by Mutation. 
3. ^ Bateson, W (1894). Materials for the Study of Variation, Treated with Especial Regard to Discontinuity in the Origin of Species. 
4. ^ ^{a b c d e} Stoltzfus, A (2006). "Mutationism and the Dual Causation of Evolutionary Change". Evol Dev 8 (3): 304–317. doi:10.1111/j.1525-142X.2006.00101.x. PMID 16686641. 
5. ^ Morgan, T. H. (1916). A Critique of the Theory of Evolution. Princeton University Press, Princeton, NJ. 
6. ^ Tax, S., and Callender, C., ed (1960). Evolution After Darwin: The University of Chicago Centennial. University of Chicago Press, Chicago. 
7. ^ Sueoka, N. (1962). "On the genetic basis of variation and heterogeneity of DNA base composition". PNAS 48 (4): 582–592. doi:10.1073/pnas.48.4.582. http://www.pnas.org/cgi/reprint/48/4/582. 
8. ^ Nei, M. (1983). "Genetic polymorphism and the role of mutation in evolution". In In: Koehn, P.K. and Nei, M.. Evolution of genes and proteins. Sinauer Association, Mass. pp. 165–190. 
9. ^ ^{a b c} Tanguy Chouard (2010). "The revenge of the hopeful monster". Nature 463 (7283): 864–867. doi:10.1038/463864a. PMID 20164895. 
10. ^ Nei, M. (2007). "The new mutation theory of phenotypic evolution". PNAS 104 (30): 12235–12242. doi:10.1073/pnas.0703349104. PMC 1941456. PMID 17640887. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1941456. 
11. ^ Nei, M. (2005). "Selectionism and Neutralism in Molecular Evolution". Molecular Biology and Evolution 22 (12): 2318–2342. doi:10.1093/molbev/msi242. PMC 1513187. PMID 16120807. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1513187. 
12. ^ Takahata, N (2007). "Molecular Clock: An Anti-neo-Darwinian Legacy". Genetics 176 (1): 1–6. doi:10.1534/genetics.104.75135. PMC 1893057. PMID 17513888. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1893057. 
13. ^ ^{a b} Stoltzfus, A and Yampolsky, L.Y. (2009). "Climbing Mount Probable: Mutation as a Cause of Nonrandomness in Evolution". J Hered 100 (5): 637–647. doi:10.1093/jhered/esp048. PMID 19625453. 
14. ^ Yampolsky, L.Y. and Stoltzfus, A (2001). "Bias in the introduction of variation as an orienting factor in evolution". Evol Dev 3 (2): 73–83. doi:10.1046/j.1525-142x.2001.003002073.x. PMID 11341676. 
15. ^ Graur, D. and Li, W-H. (2000). Fundamentals of Molecular Evolution (second edition). Sinauer Associates. ISBN 0-87893-266-6. 
16. ^ Sueoka, N. (1964). "On the evolution of informational macromolecules". In In: Bryson, V. and Vogel, H.J.. Evolving genes and proteins. Academic Press, New-York. pp. 479–496. 
17. ^ Muto, A. and Osawa, S. (1987). "The guanine and cytosine content of genomic DNA and bacterial evolution". PNAS 84 (1): 166–169. doi:10.1073/pnas.84.1.166. PMC 304163. PMID 3467347. http://www.pnas.org/cgi/reprint/84/1/166. 
18. ^ Gu, X., Hewett-Emmett, D. and Li, W-H. (1998). "Directional mutational pressure affects the amino acid composition and hydrophobicity of proteins in bacteria". Genetica 102/103: 383–391. doi:10.1023/A:1017028102013. PMID 9720290. http://xgu.zool.iastate.edu/publications/GuEtal_Genetica98.pdf. 
19. ^ Argos, P., Rossmann, M.G., Grau, U.M., Zuber, A., Frank, G. and Tratschin, J.D. (1979). "Thermal stability and protein structure". Biochemistry 18 (25): 5698–5703. doi:10.1021/bi00592a028. PMID 518863. 
20. ^ Singer, C.E. and Ames, B.N. (1970). "Sunlight ultraviolet and bacterial DNA base ratios". Science 170 (3960): 822–826. doi:10.1126/science.170.3960.822. PMID 5473414. 
21. ^ Galtier, N. and Lobry, J.R. (1997). "Relationships between genomic G+C content, RNA secondary structure, and optimal growth temperature in prokaryotes". Journal of Molecular Evolution 44 (6): 632–636. doi:10.1007/PL00006186. PMID 9169555. 
22. ^ Palmeira, L. and Guéguen, L. and Lobry, J.R. (2006). "UV-targeted dinucleotides are not depleted in light-exposed Prokaryotic genomes". Molecular Biology and Evolution 23 (11): 2214–2219. doi:10.1093/molbev/msl096. PMID 16926242. http://mbe.oxfordjournals.org/cgi/reprint/23/11/2214.