Mutationism

Mutationism refers to historical and contemporary views of evolution that emphasize the role of mutation and that are understood as alternatives to Darwinism.^[1] In the mutationist view, change may occur in discrete jumps (i.e., gradualism is not assumed), mutation is seen as the source of novelty (while selection is not seen as creative), and the direction of evolution is understood to reflect both mutation and selection.^[2]

Historical mutationism

General history

By 1909, "mutationism" was referenced as a distinctive rival of Darwinism,^[3] following the discovery and naming of "mutation" by Hugo De Vries.^[4] At that time, Darwin's mechanism of natural selection was understood to rely on hereditary blending of abundant continuous variations . However, Wilhelm Johannsen's "pure line" experiments appeared to refute this mechanism.^[5] Using true-breeding varieties of beans, each with a different size of seeds, Johannsen showed selection could be used to sort out different varieties, but selection within pure lines would not produce evolutionary changes, even though pure lines continued to generate the kind of abundant variations that Darwinians saw as the fuel for evolution.

At the same time, Hugo de Vries's careful studies of wild variants of Oenothera lamarckiana, initially published in 1901,^[4] showed that distinct new forms could arise suddenly in nature, and could be propagated for many generations without dissipation or blending. De Vries used the term "mutation" to refer to these dramatic variants, as well as any smaller variations that arise via a sudden event and are inherited stably (as distinct from unstable quantitative fluctuations). Thereafter, "mutationism" came to refer to a view of evolution emphasizing that inheritance is discrete, and that hereditary variants originate in discrete events of mutation, which have a role in shaping the outcome of evolution. The terms "saltationism" and "Mendelism" appear to be used similarly. This was contrasted with a Darwinian view in which variation is continuous, and hereditary variations emerge as masses of infinitesimal effects that are shaped by selection.

These and other early discoveries of genetics are often framed relative to a controversy between, on the one hand, early geneticists— the "Mendelians"— including William Bateson, Wilhelm Johannsen, Hugo de Vries, Thomas Hunt Morgan, and Reginald Punnett, who advocated Mendelism and mutation, and were understood as opponents of Darwin's original view, and the biometricians and their allies, who opposed Mendelism and were more faithful to Darwin's original vision.^[6] The dispute was resolved, and the eclipse of Darwinism ended, with the rise of the "Modern Synthesis" or modern neo-Darwinism from 1930 to 1950.

Neodarwinist view

While historians agree on the above generalities, they disagree on the nature of the critique of Darwinism offered by geneticists, their alternative view of evolution, and the Darwinian restoration in the modern evolutionary synthesis.^[1] In the classical view, early geneticists, upon the discovery of mutation, mistakenly assume that all mutations are large, exaggerate their importance, reject Darwin's idea of selection, and imagine an entire theory of evolution based on dramatic mutations, in which new species were created in a single step; this view gains popularity and temporarily eclipses Darwin's theory; it takes decades for scientists to come to their senses and see that genetics and selection may be combined in a way that allows gradual evolution consistent with Darwin's original vision. The classical view, which emerged in Modern Synthesis writings, presents the Modern Synthesis as the received view and mutationism as an obvious error; the decades-long delay in synthesizing genetics and Darwinism is seen as an "inexplicable embarrassment".^[7]

The nature of this synthesis was that, due to recombination in the diverse gene pool of a population, selection can shift the phenotype well beyond its initial limits, essentially creating a new form without any mutations. This argument for "the effectiveness of selection" is the centerpiece of Provine's seminal history of theoretical population genetics.^[6] It is often associated with Ronald Fisher's famous article of 1918 ^[8] and presented as a logical necessity underpinning the Modern Synthesis and all subsequent evolutionary thinking. Thus, in the classical view, scientists who look to distinctive individual mutations for the origin of novelty, rather than to selection smoothly shifting an entire distribution (of many infinitesimal variations) to fit external conditions, are seen as advocates of a failed theory. Mutationism (saltationism), along with Lamarckism and orthogenesis, are presented as anti-Darwinian "blind alleys" separate from the main line leading from Darwin to the present.^[9]

Historical view

Though the classical view is commonly repeated by scientists, it is not clear how strongly historians would defend it against revisionist claims.^[1][5][10] Gayon's Darwinism's Struggle for Survival ^[10] argues that Darwin's conception of natural selection was incompatible with Mendelian genetics, and that early geneticists are responsible for "the most important event in the history of Darwinism: the Mendelian reconstruction of the principle of selection" (289) as a force that shifts frequencies of discretely inherited types. That is, Gayon places the early geneticists, not in a blind alley, but in the middle of the genetic reformation of evolutionary thinking, validating their main complaints against Darwin's non-Mendelian view of a creative force of selection.

Provine's seminal history of theoretical population genetics ^[6] presents a version of the classical narrative, yet in the 2001 reprinting of the same work, Provine rejects the inevitability of the Modern Synthesis (which "came unraveled"), and questions both the sufficiency and the logical coherence of its selection-and-recombination-driven "gene pool" view of population genetics.^[6] Provine lists a variety of post-Synthesis findings that are not consistent with the synthetic view of population genetics presented in his 1971 analysis.

The most sympathetic view of the mutationists is given by Stoltzfus and Cable,^[1] who argue that early geneticists accepted selection, allowed gradual evolution, and laid the conceptual foundations for the genetical view of evolution that prevails today. They argue that the fusion of Darwinism and genetics that Provine describes achieved premature acceptance, but later proved untenable and is no longer the foundation of contemporary evolutionary thinking, which is better aligned with the "Mendelian-mutationism" of early geneticists.

In summary, classical historiography holds that mutationism is a failed view in which the role of mutation in evolution is misperceived, while the role of selection is wrongly dismissed. In revisionist views, the mutationists accept both mutation and selection, and assign them the same qualitative roles they are assigned today, though perhaps not the same quantitative emphasis. 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 of the publication of On the Origin of Species, mutationism (like Lamarckism) was no longer seriously considered.^[11] Nevertheless, after another 50 years, evolutionary biologists are re-considering the mutationist view.

Contemporary mutationism

With the arrival of molecular biology, scientists studying "molecular evolution" began to suggest mutational explanations for patterns such as genomic nucleotide composition,^[12] and eventually it became a characteristic of the field of molecular evolution to emphasize the role of mutation in evolution.^[13] Contemporary interest in mutationism is revealed by articles in mainstream research journals that advocate mutationist ideas, referring to Richard Goldschmidt's concept of the hopeful monster,^[14] or using the label "mutationism" or "neo-mutationism".^{[15][16][17][18][19]} Phrases such as "new thermutations" or "mutation-driven evolution"^[20] also indicate a departure from the "shifting gene frequencies" view of neo-Darwinism, in which evolution consists of establishing a new multi-locus equilibrium for the frequencies of pre-existing alleles, without new mutations.^[19]

A recent book review also refers to James A. Shapiro's view as "mutationism",^[21] but the defining feature of Shapiro's view is to treat mutation as a goal-directed (teleological) process, an idea that was not part of historical mutationism.

Instead, contemporary mutationism is more a position on the relative roles played by mutation and selection in evolution,^[22] which is partly a philosophical issue of how causes are conceived, and partly a more mechanistic issue of the regime of population genetics in which natural evolution occurs.^[23] Wagner ^[22] characterizes this position by saying that the core processes of population genetics are uncontroversial, but

"What is debatable, however, is the question what the explanatory power of each of these processes/mechanisms is. In the classic synthetic theory of evolution, which is the core of the mainstream version of evolutionary thinking, selection is the only truly causal factor, which gives direction to evolutionary change. That is to say, anything that is not a random outcome of evolution is to be explained by natural selection. "

Takahata ^[24] describes it thus:

"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."

Stoltzfus argues that the historical mutationists embraced ideas about evolutionary causes that neo-Darwinists rejected and claimed to have refuted, but which have been shown to be theoretically valid implications of population genetics, supported by evidence from comparative data and evolution experiments. One of these is that biases in variation are a cause of direction in evolution— the heresy of "orthogenesis"—, which can be argued from theoretical models ^[25][26] and empirical results.^[27] Another is that the variations used in evolution are not always infinitesimal or slight. A third, argued by Masatoshi Nei and Stoltzfus (see,^[23] is that evolution often occurs in a mutation-limited regime of evolutionary genetics rejected by the Modern Synthesis, which was based on the "shifting gene frequencies" view of polygenic, quantitative change. This position is elaborated in a review of the mathematics, history, and implications of origin-fixation models,^[28] a widely used class of models in which evolutionary change is a 2-step process of (1) the introduction of a new mutation, and (2) its subsequent fixation or loss. Such models represent a theory of change distinct from the Modern Synthesis that was not developed until 1969, based on an emerging view of molecular evolution.

If these arguments are accepted, it would mean that a variety of theoretical and empirical results, some of them well known (e.g., Lenski's experimental evolution studies ^[29]), already provide support for mutationism. Not just Nei, but authors such as Eugene Koonin argue that gene duplications and fusions, genome doublings, gene transfers, and other events common in molecular evolution are discontinuous changes whose importance supports a saltationism view and counts against Darwinism.^[30][31]

There is little evidence on the reception of mutationism among evolutionary biologists, as it rarely mentioned. Reviews of Nei's book in mainstream journals were more positive than negative: Wright,^[32] writing for the conservative journal Evolution, rejects Nei's thinking as mistaken, while Galtier,^[33] Weiss,^[34] Stoltzfus,^[23] and Wagner,^[22] while not necessarily agreeing with Nei's position, treat it as an alternative view relevant to reforming or improving evolutionary thinking on the role of mutation in evolution.

See also

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

References

Further reading

• Allen, Garland E. (1968). Thomas Hunt Morgan and the Problem of Natural Selection. Journal of the History of Biology 1: 113-139.
• Bateman, Richard M; DiMichele, William A. (2002). Generating and Filtering Major Phenotypic Novelties, NeoGoldschmidtian Saltation Revisited. In Cronk QCB, Bateman RM, Hawkins JA, eds. Developmental Genetics and Plant Evolution. London: Taylor & Francis. pp. 109–159.
• Bateson, William. (1894). Materials for the Study of Variation: Treated with Especial Regard to Discontinuity in the Origin of Species. Macmillan and Company.
• Gillham, Nicholas W. (2001). Evolution by Jumps: Francis Galton and William Bateson and the Mechanism of Evolutionary Change. Genetics 159: 1383-1392.
• Nei, Masatoshi. (2013). Mutation-Driven Evolution. Oxford University Press.
• Stoltzfus, Arlin; Cable, Kele. (2014). Mendelian-Mutationism: The Forgotten Evolutionary Synthesis. Journal of the History of Biology 47: 501-546.

External links

• Mutation, Not Natural Selection, Drives Evolution Discover magazine.