History of molecular evolution
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The history of molecular evolution starts in the early 20th century with "comparative biochemistry", but the field of
Early history
Before the rise of molecular biology in the 1950s and 1960s, a small number of biologists had explored the possibilities of using biochemical differences between species to study evolution.
The first molecular systematics research was based on immunological
Beginning in the 1950s, a few naturalists also experimented with molecular approaches—notably
While such early biochemical techniques found grudging acceptance in the biology community, for the most part they did not impact the main theoretical problems of evolution and population genetics. This would change as molecular biology shed more light on the physical and chemical nature of genes.
Genetic load, the classical/balance controversy, and the measurement of heterozygosity
At the time that molecular biology was coming into its own in the 1950s, there was a long-running debate—the classical/balance controversy—over the causes of
Muller, motivated by his concern about the effects of radiation on human populations, argued that heterosis is primarily the result of deleterious homozygous recessive alleles, the effects of which are masked when separate lines are crossed—this was the dominance hypothesis, part of what Dobzhansky labeled the classical position. Thus, ionizing radiation and the resulting mutations produce considerable genetic load even if death or disease does not occur in the exposed generation, and in the absence of mutation natural selection will gradually increase the level of homozygosity. Bruce Wallace, working with J. C. King, used the overdominance hypothesis to develop the balance position, which left a larger place for overdominance (where the heterozygous state of a gene is more fit than the homozygous states). In that case, heterosis is simply the result of the increased expression of heterozygote advantage. If overdominant loci are common, then a high level of heterozygosity would result from natural selection, and mutation-inducing radiation may in fact facilitate an increase in fitness due to overdominance. (This was also the view of Dobzhansky.)[6]
Debate continued through 1950s, gradually becoming a central focus of population genetics. A 1958 study of Drosophila by Wallace suggested that radiation-induced mutations increased the viability of previously homozygous flies, providing evidence for heterozygote advantage and the balance position; Wallace estimated that 50% of loci in natural Drosophila populations were heterozygous. Motoo Kimura's subsequent mathematical analyses reinforced what Crow had suggested in 1950: that even if overdominant loci are rare, they could be responsible for a disproportionate amount of genetic variability. Accordingly, Kimura and his mentor Crow came down on the side of the classical position. Further collaboration between Crow and Kimura led to the infinite alleles model, which could be used to calculate the number of different alleles expected in a population, based on population size, mutation rate, and whether the mutant alleles were neutral, overdominant, or deleterious. Thus, the infinite alleles model offered a potential way to decide between the classical and balance positions, if accurate values for the level of heterozygosity could be found.[7]
By the mid-1960s, the techniques of biochemistry and molecular biology—in particular
Protein sequences and the molecular clock
While evolutionary biologists were tentatively branching out into molecular biology, molecular biologists were rapidly turning their attention toward evolution.
After developing the fundamentals of protein sequencing with insulin between 1951 and 1955, Frederick Sanger and his colleagues had published a limited interspecies comparison of the insulin sequence in 1956. Francis Crick, Charles Sibley and others recognized the potential for using biological sequences to construct phylogenies, though few such sequences were yet available. By the early 1960s, techniques for protein sequencing had advanced to the point that direct comparison of homologous amino acid sequences was feasible.[11] In 1961, Emanuel Margoliash and his collaborators completed the sequence for horse cytochrome c (a longer and more widely distributed protein than insulin), followed in short order by a number of other species.
In 1962, Linus Pauling and Emile Zuckerkandl proposed using the number of differences between homologous protein sequences to estimate the time since divergence, an idea Zuckerkandl had conceived around 1960 or 1961. This began with Pauling's long-time research focus, hemoglobin, which was being sequenced by Walter Schroeder; the sequences not only supported the accepted vertebrate phylogeny, but also the hypothesis (first proposed in 1957) that the different globin chains within a single organism could also be traced to a common ancestral protein.[12] Between 1962 and 1965, Pauling and Zuckerkandl refined and elaborated this idea, which they dubbed the molecular clock, and Emil L. Smith and Emanuel Margoliash expanded the analysis to cytochrome c. Early molecular clock calculations agreed fairly well with established divergence times based on paleontological evidence. However, the essential idea of the molecular clock—that individual proteins evolve at a regular rate independent of a species' morphological evolution—was extremely provocative (as Pauling and Zuckerkandl intended it to be).[13]
The "molecular wars"
From the early 1960s, molecular biology was increasingly seen as a threat to the traditional core of evolutionary biology. Established evolutionary biologists—particularly
In 1961, Mayr began arguing for a clear distinction between functional biology (which considered
Mayr and Simpson attended many of the early conferences where molecular evolution was discussed, critiquing what they saw as the overly simplistic approaches of the molecular clock. The molecular clock, based on uniform rates of genetic change driven by random mutations and drift, seemed incompatible with the varying rates of evolution and environmentally-driven adaptive processes (such as
Gene-centered view of evolution
Though not directly related to molecular evolution, the mid-1960s also saw the rise of the
The neutral theory of molecular evolution
The intellectual threat of molecular evolution became more explicit in 1968, when Motoo Kimura introduced the
Kimura's theory—described only briefly in a letter to Nature—was followed shortly after with a more substantial analysis by
King and Jukes' paper, especially with the provocative title, was seen as a direct challenge to mainstream neo-Darwinism, and it brought molecular evolution and the neutral theory to the center of evolutionary biology. It provided a mechanism for the molecular clock and a theoretical basis for exploring deeper issues of molecular evolution, such as the relationship between rate of evolution and functional importance. The rise of the neutral theory marked synthesis of evolutionary biology and molecular biology—though an incomplete one.[24]
With their work on firmer theoretical footing, in 1971 Emile Zuckerkandl and other molecular evolutionists founded the Journal of Molecular Evolution.
The neutralist-selectionist debate and near-neutrality
The critical responses to the neutral theory that soon appeared marked the beginning of the neutralist-selectionist debate. In short, selectionists viewed natural selection as the primary or only cause of evolution, even at the molecular level, while neutralists held that neutral mutations were widespread and that genetic drift was a crucial factor in the evolution of proteins. Kimura became the most prominent defender of the neutral theory—which would be his main focus for the rest of his career. With Ohta, he refocused his arguments on the rate at which drift could fix new mutations in finite populations, the significance of constant protein evolution rates, and the functional constraints on protein evolution that biochemists and molecular biologists had described. Though Kimura had initially developed the neutral theory partly as an outgrowth of the classical position within the classical/balance controversy (predicting high genetic load as a consequence of non-neutral mutations), he gradually deemphasized his original argument that segregational load would be impossibly high without neutral mutations (which many selectionists, and even fellow neutralists King and Jukes, rejected).[25]
From the 1970s through the early 1980s, both selectionists and neutralists could explain the observed high levels of heterozygosity in natural populations, by assuming different values for unknown parameters. Early in the debate, Kimura's student Tomoko Ohta focused on the interaction between natural selection and genetic drift, which was significant for mutations that were not strictly neutral, but nearly so. In such cases, selection would compete with drift: most slightly deleterious mutations would be eliminated by natural selection or chance; some would move to fixation through drift. The behavior of this type of mutation, described by an equation that combined the mathematics of the neutral theory with classical models, became the basis of Ohta's nearly neutral theory of molecular evolution.[26]
In 1973, Ohta published a short letter in Nature
Between then and the early 1990s, many studies of molecular evolution used a "shift model" in which the negative effect on the fitness of a population due to deleterious mutations shifts back to an original value when a mutation reaches fixation. In the early 1990s, Ohta developed a "fixed model" that included both beneficial and deleterious mutations, so that no artificial "shift" of overall population fitness was necessary.
Microbial phylogeny
While early work in molecular evolution focused on readily sequenced proteins and relatively recent evolutionary history, by the late 1960s some molecular biologists were pushing further toward the base of the tree of life by studying highly conserved nucleic acid sequences.
Work on microbial phylogeny also brought molecular evolution closer to
References
- ^ Dobzhanski, Sturtevant, 1937
- ^ Dietrich, "Paradox and Persuasion", pp. 90-91; Zuckerkandl, "On the Molecular Evolutionary Clock", p. 34
- ^ Dietrich, "Paradox and Persuasion", pp. 90-91; Morgan, "Emile Zuckerkandl, Linus Pauling, and the Molecular Evolutionary Clock", pp. 161-162.
- ^ Hagen, "Naturalists, Molecular Biologists, and the Challenges of Molecular Evolution", pp. 335-339
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 25-28
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 26-31
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 33-41
- PMID 17248176.
- PMID 5968643.
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 42-45
- ^ Hagen, "Naturalists, Molecular Biologists, and the Challenge of Molecular Evolution", pp. 323-325
- ^ Zuckerkandl, "On the Molecular Evolutionary Clock", pp. 34-35
- ^ Dietrich, "Paradox and Persuasion", pp. 91-94
- ^ Dietrich, "Paradox and Persuasion", pp. 94-100
- ^ Wilson, Naturalist, pp. 219-237
- PMID 14471768.
- ^ Hagen, "Naturalists, Molecular Biologists, and the Challenges of Molecular Evolution", pp. 333-335
- PMID 14223586.
- ^ Dietrich, "Paradox and Persuation", pp. 95-98; Hagen, "Naturalists, Molecular Biologists, and the Challenges of Molecular Evolution", pp. 330-332
- ^ Motoo Kimura, [Evolutionary Rate at the Molecular Level", Nature, Vol. 217 (1968), pp. 624-626
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 46-50
- PMID 5767777.
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 50-54
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 54, 57-58
- ^ Dietrich, "The Origins of the Neutral Theory of Molecular Evolution", pp. 54-55
- ^ Ohta, "The current significance and standing of neutral and nearly neutral theories", pp. 673-674
- S2CID 4226804.
- PMID 8813019., pp 130-131
- ^ Ohta and Gillispie, "Development of Neutral and Nearly Neutral Theories", pp. 135-136
- ^ Ohta, "The current significance and standing of neutral and nearly neutral theories", p. 674
- ^ Sapp, Genesis, pp. 224-228
- ^ Sapp, Genesis, pp. 230-233
Notes
- Dietrich, Michael R. "The Origins of the Neutral Theory of Molecular Evolution." Journal of the History of Biology, Vol. 27, No. 1 (Spring 1994), pp 21–59
- Dietrich, Michael R. (1998). "Paradox and Persuasion: Negotiating the Place of Molecular Evolution within Evolutionary Biology". Journal of the History of Biology. 31 (1): 85–111. S2CID 29935487.
- Crow, James F. "Motoo Kimura, 13 November 1924 - 13 November 1994." Biographical Memoirs of Fellows of the Royal Society, Vol. 43 (November 1997), pp 254–265
- Hagen, Joel B. (1999). "Naturalists, Molecular Biologists, and the Challenge of Molecular Evolution". Journal of the History of Biology. 32 (2): 321–341. S2CID 26994015.
- Kreitman, Martin. "The neutralist-selectionist debate: The neutral theory is dead. Long live the neutral theory", BioEssays, Vol. 18, No. 8 (1996), pp. 678–684
- Morgan, Gregory J. (1998). "Emile Zuckerkandl, Linus Pauling, and the Molecular Evolutionary Clock, 1959-1965". Journal of the History of Biology. 31 (2): 155–178. S2CID 5660841.
- Ohta, Tomoko. "The neutralist-selectionist debate: The current significance and standing of neutral and nearly neutral theories", BioEssays, Vol. 18, No. 8 (1996), pp. 673–677
- Sapp, Jan. Genesis: The Evolution of Biology. New York: Oxford University Press, 2003. ISBN 0-19-515618-8
- ISBN 0-446-67199-1
- S2CID 3616497.
External links
- Perspectives on Molecular Evolution - maintained by historian of science Michael R. Dietrich