The DOI matches its Crossref record; 74 of the 74 references it cites were found in a registry or an index; 1 of the 98 sources its claims cite were checked for support.
The modern molecular clock
Abstract
The discovery of the molecular clock--a relatively constant rate of molecular evolution--provided an insight into the mechanisms of molecular evolution, and created one of the most useful new tools in biology. The unexpected constancy of rate was explained by assuming that most changes to genes are effectively neutral. Theory predicts several sources of variation in the rate of molecular evolution. However, even an approximate clock allows time estimates of events in evolutionary history, which provides a method for testing a wide range of biological hypotheses ranging from the origins of the animal kingdom to the emergence of new viral epidemics.
Overview
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Written from the paper’s full text.
TL;DR
The molecular clock—a relatively constant rate of molecular evolution—was unexpected but is broadly explained by neutral and nearly neutral theory, and it provides a universal tool for dating evolutionary events. However, the clock is “sloppy” and rates vary among lineages, so molecular dates must be treated with appropriate confidence intervals and caution.
Key findings
- Zuckerkandl and Pauling found a strikingly linear accumulation of amino-acid differences over evolutionary time, with each protein having a characteristic rate: histones were exceptionally slow, cytochrome c was faster but slower than haemoglobins, and fibrinopeptides were faster still; Kimura and Ohta explained this by suggesting most amino-acid changes are effectively neutral.
- Rate variation arises through mutation rate, population size, and selective coefficients; examples include murid rodents evolving two to three times faster than hominid primates, and HIV evolving around a million times faster than mammalian genomes.
- Molecular dates can conflict with fossil dates: molecular dates for the origins of animal phyla and orders of mammals and birds are generally twice as old as fossil dates, and published molecular dates for the rodent–primate split vary by as much as 100%.
- A practical application: molecular clock dates place the last common ancestor of the main pandemic HIV strain in the 1930s, countering claims that the virus spread through contaminated polio vaccine in the 1950s.
Methods
- Review article synthesizing the history, theory, and methods of molecular dating; no new primary data or analyses are presented.
- Discusses calibration approaches (fossil record, biogeography, sample dates for viruses), substitution models, and clock tests (relative rates test, Tajima test, likelihood ratio test), plus maximum likelihood and Bayesian methods.
- Uses examples from proteins, Hawaiian island birds and fruitflies, vertebrates, and viruses to illustrate rate constancy and variation.
Limitations
- The paper states that the molecular clock is probabilistic and “sloppy,” with overdispersed substitution intervals adding large confidence intervals; lineage effects can systematically bias date estimates.
- It notes operational errors: uncertain phylogenies, calibration-point errors, and biased genetic-distance estimates; clock tests lack power for shorter or slowly evolving sequences.
- It states that few studies present confidence intervals that accurately portray clock variance, and that molecular dates are often point estimates; as a review, it does not resolve these issues with new data (evident from text).
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Claims the paper makes
56 Not checked yet · 22 Own interpretation · 13 No basis given · 2 Own method · 1 Supported so far
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In the paper
“In fact, the molecular clock is generally even sloppier: observations indicate that the pattern of substitution intervals for many genes has a broader distribution, which might be described as an 'overdispersed' Poisson distribution 11,13,14 .”
What the sources say
- Not checked yetcites [11] Gillespie, J. H. The Causes of Molecular Evolution (Oxford University Press, Oxford, UK, 1991).
- Not checked yetcites [13] Bickel, D. R. Implications of fluctuations in substitution rates: impact on the uncertainty of branch lengths and on relative-rate tests. J. Mol. Evol. 50, 381–390 (2000). source
- Supportedcites [14] Cutler, D. J. Estimating divergence times in the presence of an overdispersed molecular clock. Mol. Biol. Evol. 17, 1647–1660 (2000). source
The Introduction describes overdispersion as substitution counts with variance greater than the Poisson expectation and explains that a variable-rate Poisson process can produce the same broader distribution. In the empirical analysis (Performance Evaluation), the constant-rate Poisson model is rejected and one locus has an inferred index of dispersion nearly 20 times the Poisson expectation. The paper also models variation in the times between substitutions, consistent with the citing sentence’s description of substitution intervals. (LLM, conf=0.88)
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In the paper
“The variation in rate of molecular evolution between lineages warns against using a calibration rate calculated for one lineage to date another, often distantly related, lineage 1,28,48 .”
What the sources say
- Not checked yetcites [1] Smith, A. B. & Peterson, K. J. Dating the time of origin of major clades: molecular clocks and the fossil record. Annu. Rev. Earth Planet. Sci. 30, 65–88 (2002). A review of the controversy surrounding dates for the Cambrian explosion of animal phyla and the early Tertiary radiation of modern mammals and birds. Written by a palaeontologist and a molecular geneticist, this review takes a critical look at the reliability of both fossil and molecular dates. source
- Not checked yetcites [28] Bromham, L. D., Rambaut, A., Hendy, M. D. & Penny, D. he power of relative rates tests depends on the data. J. Mol. Evol. 50, 296–301 (2000). source
- Not checked yetcites [48] Bromham, L. D., Phillips, M. J. & Penny, D. Growing up with dinosaurs: molecular dates and the mammalian radiation. Trends Ecol. Evol. 14, 113–118 (1999). source
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In the paper
“The molecular clock arises from the observation that the amount of difference between the DNA of two species is a function of the time since their evolutionary separation.”
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In the paper
“The choice of calibration date is crucial to the accuracy of molecular dates, as shown by the difference in date estimates from studies using the same data and methods but different calibration dates 48 .”
What the sources say
- Not checked yetcites [48] Bromham, L. D., Phillips, M. J. & Penny, D. Growing up with dinosaurs: molecular dates and the mammalian radiation. Trends Ecol. Evol. 14, 113–118 (1999). source
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In the paper
“However, there is, as yet, no evidence that environmental temperature influences the rate of molecular evolution 40,41 .”
What the sources say
- Not checked yetcites [40] Bromham, L. & Cardillo, M. Testing the link between the latitudinal gradient in species richness and rates of molecular evolution. J. Evol. Biol. 16, 200–207 (2003). source
- Not checked yetcites [41] Held, C. No evidence for slow-down of molecular substitution rates at subzero temperatures in Antarctic serolid isopods (Crustacea, Isopoda, Serolidae). Polar Biol. 24, 497–501 (2001). source
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In the paper
“The rate of accumulation of these neutral mutations would be influenced only by the mutation rate, and so would be relatively constant, as long as the base mutation rate remained unchanged (BOX 3).”
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In the paper
“In addition, the strength of selection on particular sites can change, producing bursts of substitutions as a molecule is adapted to a new role or responds to changes in another part of the genome.”
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In the paper
“But molecular dates for the origins of animal phyla 27 and orders of mammals and birds 68 are generally twice as old as the dates of origin indicated by the fossil record.”
What the sources say
- Not checked yetcites [27] Bromham, L., Rambaut, A., Fortey, R., Cooper, A. & Penny, D. Testing the Cambrian explosion hypothesis by using a molecular dating technique. Proc. Natl Acad. Sci. USA 95, 12386–12389 (1998). source
- Not checked yetcites [68] Madsen, O. et al.Parallel adaptive radiations in two major clades of placental mammals. Nature 409, 610–614 (2001). Used the quartet method which uses several calibration dates to allow for differences in substitution rate between lineages to support the hypothesis that modern mammals arose long before the final extinction of the dinosaurs. source
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In the paper
“Therefore, the fixation of nearly-neutral alleles of small selective effect is expected to be greatest in small populations 23,24 .”
What the sources say
- Not checked yetcites [23] Ohta, T. Very slightly deleterious mutations and the molecular clock. J. Mol. Evol. 26, 1–6 (1987). source
- Not checked yetcites [24] Ohta, T. Near-neutrality in evolution of genes and gene regulation. Proc. Natl Acad. Sci. USA 99, 16134–16137 (2002). The most recent exposition of the nearly-neutral model, in which the effects of weak selection depend both on the selection coefficient of the mutation and the size of the population in which the mutant occurs. source
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In the paper
“This is a fundamental result; it predicts that the long-term rate of neutral molecular evolution in species is the same as the neutral mutation rate in individuals.”
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In the paper
“The unexpected constancy of rate was explained by assuming that most changes to genes are effectively neutral.”
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In the paper
“For example, molecular clock dates that place the last common ancestor of the main pandemic strain of human immunodeficiency virus (HIV) in the 1930s have been used to counter claims that the virus was spread through the distribution of contaminated polio vaccine in the 1950s (allegedly manufactured using tissue from chimpanzees infected with simian immunodeficiency virus) 2 .”
What the sources say
- Not checked yetcites [2] Korber, B. et al.Timing the ancestor of the HIV-1 pandemic strains. Science 288, 1789–1796 (2000). source
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In the paper
“The discovery of the molecular clock - a relatively constant rate of molecular evolution provided an insight into the mechanisms of molecular evolution, and created one of the most useful new tools in biology.”
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In the paper
“Theory predicts several sources of variation in the rate of molecular evolution.”
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In the paper
“However, extrapolation has few constraints on the variances and biases, so uncertainty increases with the distance between the calibration point and the estimated node.”
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In the paper
“Selection of the substitution model governs the accuracy of genetic distance estimates and is therefore crucial to the accuracy of molecular dating.”
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In the paper
“However, this approach will fail to count 'multiple hits' (repeated changes), so a model of sequence evolution is needed to estimate the true number of substitutions that have occurred, using the observed number 67 .”
What the sources say
- Not checked yetcites [67] Page, R. D. M. & Holmes, E. C. Molecular Evolution: a Phylogenetic Approach (Blackwell Science, Oxford, UK, 1998).
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In the paper
“The reliability of all molecular clock methods depends on the accuracy with which genetic distance is estimated, and on the appropriateness of the calibration rate.”
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In the paper
“However, even an approximate clock allows time estimates of events in evolutionary history, which provides a method for testing a wide range of biological hypotheses ranging from the origins of the animal kingdom to the emergence of new viral epidemics.”
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In the paper
“Even within mammalian cells, different replication and repair enzymes vary in mutation rate: mitochondrial DNA is copied by DNA polymeraseγ , which has a higher error rate than other mammalian DNA polymerases,and this contributes to the higher mutation rate of mitochondrial genes over nuclear genes.”
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“Small populations are more severely affected by stochastic fluctuations in allele frequencies, so genetic drift (random sampling error on allele frequencies) can overpower selection for alleles with small selection coefficients.”
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In the paper
“This constancy of rates is broadly supported by observation: the amount of divergence between genes tends to increase with the time since evolutionary separation, and in many cases the increase seems linear, as in the classic example of globin genes 3 .”
What the sources say
- Not checked yetcites [3] Zuckerkandl, E. & Pauling, L. in Horizons in Biochemistry (eds Kasha, M. & Pullman, B.) 189–225 (Academic Press, New York, 1962).
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In the paper
“According to the neutral theory of Kimura 4,72 (FIG. 1b) , the overall mutation rate ( µ ) is the sum of deleterious ( µ -), neutral ( µ º), and positive ( µ + ) mutations, µ = µ - +µ º +µ + .”
What the sources say
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In the paper
“This is consistent with the observations that ECTOTHERMS have lower substitution rates than ENDOTHERMS 36 , that smaller-bodied species of vertebrates with faster metabolic rates have higher substitution rates than larger-bodied species 35,37-39 and that animal mitochondria, which are at the site of oxidative phosporylation, have a higher rate of molecular evolution than nuclear rates 34 (it would”
What the sources say
- Not checked yetcites [36] Martin, A. P. Metabolic rate and directional nucleotide substitution in animal mitochondrial DNA. Mol. Biol. Evol. 12, 1124–1131 (1995).
- Not checked yetcites [35] Martin, A. P. & Palumbi, S. R. Body size, metabolic rate, generation time and the molecular clock. Proc. Natl Acad. Sci. USA 90, 4087–4091 (1993). Showed a relationship between body size and the rate of molecular evolution for vertebrates using estimates of absolute substitution rates. This paper showed that the life history of a species must influence the rate of molecular evolution. source
- Not checked yetcites [37] Bromham, L., Rambaut, A. & Harvey, P. H. Determinants of rate variation in mammalian DNA sequence evolution. J. Mol. Evol. 43, 610–621 (1996). source
- Not checked yetcites [38] Bromham, L. Molecular clocks in reptiles: life history influences rate of molecular evolution. Mol. Biol. Evol. 19, 302–309. (2002). source
- Not checked yetcites [39] Mooers, A. Ø. & Harvey, P. H. Metabolic rate, generation time and the rate of molecular evolution in birds. Mol. Phylogenet. Evol. 3, 344–350 (1994). source
- Not checked yetcites [34] Rand, D. M. Thermal habit, metabolic rate and the evolution of mitochondrial DNA. Trends Ecol. Evol. 9, 125–131 (1994). source
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In the paper
“An early and unexpected finding from the molecular revolution was the discovery that a given protein has a characteristic rate of evolution, but that genes differ in their characteristic rates.”
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In the paper
“Because of the universality of DNA (or RNA), molecular clocks can reach all timescales of evolution, from population divergences to the last common ancestor of the five kingdoms of life.”
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In the paper
“Conversely, many palaeontologists suggest that the discrepancy between molecular and palaeontological dates shows that molecular clocks can be systematically inaccurate, because some process associated with explosive radiations could speed the molecular clock 69,70 (although no supporting evidence has yet been found for this hypothesis 49 ).”
What the sources say
- Not checked yetcites [69] Conway Morris, S. Early metazoan evolution: reconciling paleontology and molecular biology. Am. Zool. 38, 867–877 (1998). source
- Not checked yetcites [70] Valentine, J., Jablonski, D. & Erwin, D. Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development 126, 851–859 (1999). source
- Not checked yetcites [49] Bromham, L. Molecular clocks and explosive radiations. J. Mol. Evol. (in the press). source
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In the paper
“For example, murid rodents (rats, mice and hamsters) have less efficient excisionrepair mechanisms than humans 31 and this is consistent with the higher rate of molecular evolution in murid rodents than in hominids 32 .”
What the sources say
- Not checked yetcites [31] Hart, R. W. & Setlow, R. B. Correlation between deoxyribonucleic acid excision-repair and life-span in a number of mammal species. Proc. Natl Acad. Sci. USA 71, 2169–2173 (1974). source
- Not checked yetcites [32] Li, W. -H., Ellesworth, D. L., Krushkal, J., Chang, B. H. -J. & Hewett-Emmett, D. Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis. Mol. Phylogenet. Evol. 5, 182–187 (1996). source
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In the paper
“Some researchers suggest that the pace and degree of change in explosive radiations is too great to be explained by Darwinian MICROEVOLUTIONARY processes, and that special mechanisms must be invoked,such as rapid change by developmental macromutations involving the HOX GENE COMPLEX 70,71 .”
What the sources say
- Not checked yetcites [70] Valentine, J., Jablonski, D. & Erwin, D. Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development 126, 851–859 (1999). source
- Not checked yetcites [71] Carroll, R. C. Towards a new evolutionary synthesis. Trends Ecol. Evol. 15, 27–32 (2000). source
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In the paper
“However, it could be related to population size effects if rapidly speciating lineages undergo frequent population subdivision 40 .”
What the sources say
- Not checked yetcites [40] Bromham, L. & Cardillo, M. Testing the link between the latitudinal gradient in species richness and rates of molecular evolution. J. Evol. Biol. 16, 200–207 (2003). source
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In the paper
“if the rate of molecular evolution is relatively constant, then the amount of genetic difference between two species gives a measure of the time since their evolutionary separation”
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In the paper
“Mutation rate clearly varies between taxa 29 and much of this variation is due to differences in repair equipment (biochemical factors).”
What the sources say
- Not checked yetcites [29] Drake, J., Charlesworth, B., Charlesworth, D. & Crow, J. Rates of spontaneous mutation. Genetics 148, 1667–1686 (1998). Observable mutation rates, when measured per genome per generation, are remarkably similar across widely divergent organisms, indicating that natural selection might shape optimum mutation rates. source
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In the paper
“It is possible that the population size effect could also account for the intriguing association between the diversification rate of flowering plant lineages (speciation minus extinction) and rates of molecular evolution 46 .”
What the sources say
- Not checked yetcites [46] Barraclough, T. G. & Savolainen, V. Evolutionary rates and species diversity in flowering plants. Evolution 55, 677–683 (2001). source
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In the paper
“So, the nearly neutral theory describes how the rate of molecular evolution can vary not only with changes in the mutation rate, but also through the changing balance between selection and drift.”
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In the paper
“There are three approaches to allowing for the variation in the rate of molecular evolution.”
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In the paper
“However, these clock tests lack power for shorter sequences (or genes with low rates of change) and will detect only a relatively low proportion of cases of rate variation for the types of sequence that are typically used in molecular clock studies 28 .”
What the sources say
- Not checked yetcites [28] Bromham, L. D., Rambaut, A., Hendy, M. D. & Penny, D. he power of relative rates tests depends on the data. J. Mol. Evol. 50, 296–301 (2000). source
plaindirect- Asserted: passes — The authors put it forward as true.
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“A likelihood ratio test is used to compare the fit of a single substitution rate with a multiple-rate model.”
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Mutations are divided into three categories: mutations for which selection is the predominant force (4N e σ s > 3); nearly neutral mutations, which are governed by both selection and drift (3 ≥ 4N e σ s ≤ 0.2); and effectively neutral mutations, the fate of which is determined only by drift (4N e σ s < 0.2).”
What the sources say
- Not checked yetcites [22] Ohta, T. & Kimura, M. On the constancy of the evolutionary rate of cistrons. J. Mol. Evol. 1, 18–25 (1971). source
- Not checked yetcites [23] Ohta, T. Very slightly deleterious mutations and the molecular clock. J. Mol. Evol. 26, 1–6 (1987). source
- Not checked yetcites [24] Ohta, T. Near-neutrality in evolution of genes and gene regulation. Proc. Natl Acad. Sci. USA 99, 16134–16137 (2002). The most recent exposition of the nearly-neutral model, in which the effects of weak selection depend both on the selection coefficient of the mutation and the size of the population in which the mutant occurs. source
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may state two separate claims as one.
In the paper
“Second, the nearly neutral theory predicts that the rate of molecular evolution is influenced by mutation rate, population size and the relative proportions of sites with different selective coefficients; these factors might differ between genes, between species and over time, potentially resulting in consistent bias in date estimates 28 .”
What the sources say
- Not checked yetcites [28] Bromham, L. D., Rambaut, A., Hendy, M. D. & Penny, D. he power of relative rates tests depends on the data. J. Mol. Evol. 50, 296–301 (2000). source
hedgeddirect- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“Slightly deleterious mutations will tend to be removed by selection in very large populations; however, they can be fixed by chance in smaller populations in which selection can be overpowered by random sampling events (GENETIC DRIFT) .”
What the sources say
- Not checked yetcites [22] Ohta, T. & Kimura, M. On the constancy of the evolutionary rate of cistrons. J. Mol. Evol. 1, 18–25 (1971). source
- Not checked yetcites [23] Ohta, T. Very slightly deleterious mutations and the molecular clock. J. Mol. Evol. 26, 1–6 (1987). source
- Not checked yetcites [24] Ohta, T. Near-neutrality in evolution of genes and gene regulation. Proc. Natl Acad. Sci. USA 99, 16134–16137 (2002). The most recent exposition of the nearly-neutral model, in which the effects of weak selection depend both on the selection coefficient of the mutation and the size of the population in which the mutant occurs. source
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“Molecular dates for Hemignathus (panel b ) and Drosophila (panel c ) confirm this order of colonization, and produce a remarkably linear relationship between genetic divergence and time when DNA distance is plotted against island age.”
What the sources say
- Not checked yetcites [10] Fleischer, R. C., McIntosh, C. E. & Tarr, C. L. Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K-Ar based ages of the Hawaiian islands to estimate molecular evolutionary rates. Mol. Ecol. 7, 533–545 (1998). source
boostedcorrelational- Asserted: passes — The authors put it forward as true.
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Molecular evolutionary theory has led to the prediction that species can differ in their rate of molecular evolution through changes to traits that influence mutation rate, population size or selective coefficients, but the measurable effect of these predicted influences has only recently begun to be investigated for a wide range of taxa.”
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper may give no reason why it holds. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Several dates can be used to fit a linear relationship between genetic distance and time, which might subsequently be used to estimate the rate of molecular evolution 62 or the time of origin of the last common ancestor of all included samples 2 .”
What the sources say
- Not checked yetcites [62] Shankarappa, R. et al. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73, 10489–10502 (1999). source
- Not checked yetcites [2] Korber, B. et al.Timing the ancestor of the HIV-1 pandemic strains. Science 288, 1789–1796 (2000). source
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“Estimating maximum and minimum possible rates for a given data set requires several calibration dates, which are not always available, and gives conservative assessments of molecular dates that are suitable only for rejecting particular hypotheses as being inconsistent with the data 55 .”
What the sources say
- Not checked yetcites [55] Bromham, L. D. & Hendy, M. D. Can fast early rates reconcile molecular dates to the Cambrian explosion? Proc. R. Soc. Lond. B 267, 1041–1047 (2000). source
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The high variance that arises from residual effects makes date estimates imprecise, but lineage effects, in which different species have different characteristic rates, might bias date estimates - that is, estimates based on the assumption of a constant rate might produce consistently over- or under-estimated dates.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“Failure to detect rate variation can cause systematic error in date estimates, because undetected rate variation can lead to consistently overestimated dates of divergence 28 .”
What the sources say
- Not checked yetcites [28] Bromham, L. D., Rambaut, A., Hendy, M. D. & Penny, D. he power of relative rates tests depends on the data. J. Mol. Evol. 50, 296–301 (2000). source
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“Similar methods have been developed that use Bayesian statistics to select the most likely parameters of molecular evolution for a set of viral sequences, including the substitution rates and timing of ancestral nodes 64 .”
What the sources say
- Not checked yetcites [64] Drummond, A., Pybus, O. G. & Rambaut, A. Inference of viral evolutionary rates from molecular sequences. Adv. Parasitol. (in the press). A review of the methods used to estimate substitution rates in viruses, including estimating molecular dates when rates vary.
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, the method relies on the validity of many assumptions, some of which might be inappropriate for the data being tested (such as the assumption that a constant rate of lineage origination and extinction, counter to the proposed 'explosion') (BOX 2).”
hedged- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Compounding these residual and lineage errors in the clock are operational errors in measuring the rate of molecular evolution, which include uncertainty in the relationships between taxa (the evolutionary tree), errors in calibration points and uncertainties in the mechanism of evolution 1,49 .”
What the sources say
- Not checked yetcites [1] Smith, A. B. & Peterson, K. J. Dating the time of origin of major clades: molecular clocks and the fossil record. Annu. Rev. Earth Planet. Sci. 30, 65–88 (2002). A review of the controversy surrounding dates for the Cambrian explosion of animal phyla and the early Tertiary radiation of modern mammals and birds. Written by a palaeontologist and a molecular geneticist, this review takes a critical look at the reliability of both fossil and molecular dates. source
- Not checked yetcites [49] Bromham, L. Molecular clocks and explosive radiations. J. Mol. Evol. (in the press). source
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“All molecular clock methods rely on accurate estimates of the genetic distance between sequences, and, in some cases, this measurement might be biased.”
hedgedconditional- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds. It may state two separate claims as one.
The paper relies on this without support.
Molecular dates are frequently presented as point estimates, or with sample errors that represent the difference between estimates in the same study.
“Part of the difficulty of assessing the reliability of molecular clocks is that molecular dates are frequently presented as point estimates, or with sample errors that represent the difference between estimates in the same study.”
The paper relies on this without support.
Few studies present molecular date estimates with confidence intervals that accurately portray the variance in the clock due to the sloppiness of the tick rate, or the lineage variation in rates.
“Few studies present molecular date estimates with confidence intervals that accurately portray the variance in the clock due to the sloppiness of the tick rate, or the lineage variation in rates.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Actually, single fossils may also bear their load of uncertainty in taxonomy identification and geological ages (11).”
From The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils? (2004) · cites this paper as [11]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Box 4 | The nearly neutral theory: population size and the molecular clock · p. 6
“nearly neutral mutations, which are governed by both selection and drift (3 ≥ 4N e σ s ≤ 0.2)”
§ Box 4 | The nearly neutral theory: population size and the molecular clock · p. 6
“effectively neutral mutations, the fate of which is determined only by drift (4N e σ s < 0.2)”
Citations
Cites
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“A more promising approach is to explicitly model rate variation over the phylogen”
Background
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Cited by
Sorted by citations
Items 101–200 of 615
Goodier, S., Cotterill, F. P. D., O’Ryan, C., Skelton, P., & de Wit, M. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028775 · Cited by 115
“However, despite this large uncertainty, the estimated dates provide reliable evidence to discuss the evolutionary history of Hydrocynus since even approximate estimates can be used to explain biogeographical history [37,38,62,63].”
BackgroundAntonelli, A., Quijada‐Mascareñas, A., Crawford, A. J., Bates, J. M., Velazco, P. M., & Wüster, W. (2009) · Wiley eBooks · doi:10.1002/9781444306408.ch24 · Cited by 115
Fossil Record and Age of the Asteridae
Martínez‐Millán, M. (2010) · The Botanical Review · doi:10.1007/s12229-010-9040-1 · Cited by 112
“…with the increase in computational power, correlated new algorithms, and the better understanding of genome evolution and of phylogenetics, the interest in molecular dating has increased at an unprecedented rate (see Bromham & Penny, 2003; Sanderson et al., 2004; Welch & Bromham, 2005 for reviews).”
BackgroundCounting human somatic cell replications: Methylation mirrors endometrial stem cell divisions
Kim, J. Y., Tavaré, S., & Shibata, D. K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503976102 · Cited by 106
Mitochondrial whims: metabolic rate, longevity and the rate of molecular evolution
Galtier, N., Jobson, R. W., Nabholz, B., Glémin, S., & Blier, P. U. (2009) · Biology Letters · doi:10.1098/rsbl.2008.0662 · Cited by 106
Genome-Wide Molecular Clock and Horizontal Gene Transfer in Bacterial Evolution
Novichkov, P. S., Omelchenko, M. V., Gelfand, M. S., Mironov, A. A., Wolf, Y. I., & Koonin, E. V. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.19.6575-6585.2004 · Cited by 102
“The classical molecular clock concept holds that the sequence of a given gene (protein) evolves at a constant rate as long as its biological function remains unchanged (5, 26, 56, 57).”
BackgroundBoykin, L. M., Bell, C. D., Evans, G. A., Small, I., & Barro, P. J. D. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-228 · Cited by 101
“Early criticisms of the molecular clock were directed at the assumption that the rates of evolution were assumed equal across the entire phylogeny [22,23].”
BackgroundNygren, K., Strandberg, R., Wållberg, A., Nabholz, B., Gustafsson, T., García, D., Cano, J., Guarro, J., & Johannesson, H. (2011) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.03.023 · Cited by 101
Perry, B. W., Card, D. C., McGlothlin, J. W., Pasquesi, G. I. M., Adams, R. H. J., Schield, D. R., Hales, N. R., Corbin, A. B., Demuth, J. P., Hoffmann, F. G., et al. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy157 · Cited by 101
“Variation in substitution rates has been linked to variation in recombination rate, efficacy of DNA repair, and life history traits such as body size or generation time (Martin and Palumbi 1993; Bromham 2002; Bromham and Penny 2003).”
BackgroundLiao, J., Guo, X., Weller, D. L., Pollak, S., Buckley, D. H., Wiedmann, M., & Cordero, O. X. (2021) · Nature Microbiology · doi:10.1038/s41564-021-00935-7 · Cited by 100
Detecting the Node-Density Artifact in Phylogeny Reconstruction
Venditti, C., Meade, A., & Pagel, M. D. (2006) · Systematic Biology · doi:10.1080/10635150600865567 · Cited by 100
“(Bromham, 2003; Bromham and Penny, 2003; Bromham et al., 2002).”
BackgroundSochor, M., Vašut, R. J., Sharbel, T. F., & Trávníček, B. (2015) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2015.04.007 · Cited by 97
The emerging field of geogenomics: Constraining geological problems with genetic data
Baker, P. A., Fritz, S. C., Dick, C. W., Eckert, A. J., Horton, B. K., Manzoni, S., RIBAS, C. C., Garzione, C. N., & Battisti, D. S. (2014) · Earth-Science Reviews · doi:10.1016/j.earscirev.2014.04.001 · Cited by 95
“It is the responsibility of the researcher to fully report uncertainty associated with time estimates (Bromham and Penny, 2003; Graur and Martin, 2004; Parham, 2012).”
BackgroundWritten in stone: fossils, genes and evo–devo
Raff, R. A. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2225 · Cited by 97
“Correct identification of orthologues in cases of gene duplication and divergence is vital, as is the fact that not all molecular clocks 'tick' (accumulate nucleotide substitutions) at the same rat”
BackgroundLalevée, S., Anno, Y.-N., Chatagnon, A., Samarut, É., Poch, O., Laudet, V., Benoit, G., Lecompte, O., & Rochette‐Egly, C. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.263681 · Cited by 94
Segmentation, metamerism and the Cambrian explosion
Couso, J. P. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.072425jc · Cited by 100
ACCUMULATING DOBZHANSKY-MULLER INCOMPATIBILITIES: RECONCILING THEORY AND DATA
Welch, J. J. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01695.x · Cited by 94
Li, F., Kuo, L., Pryer, K. M., & Rothfels, C. J. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw167 · Cited by 93
“Rates of molecular evolution vary dramatically among organismal lineages and across genomes (Bromham and Penny 2003) and understanding what causes this rate variation is a fundamental topic in evolutionary biology (Lanfear et al.”
BackgroundOn the instability and evolutionary age of deep-sea chemosynthetic communities
Vrijenhoek, R. C. (2012) · Deep Sea Research Part II Topical Studies in Oceanography · doi:10.1016/j.dsr2.2012.12.004 · Cited by 93
“DNA repair mechanisms, and recombination rates (Bromham and Penny, 2003; Kumar, 2005).”
BackgroundDefining Pathogenic Bacterial Species in the Genomic Era
Georgiades, K., & Raoult, D. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2010.00151 · Cited by 92
“For example, a single bacterial species may include strains with >70% DNA/DNA hybridization and a change in the melting temperature of the DNA hybrids of <5°C (Wayne, 1987; Rossello-Mora and Amann, 2001).”
RetractedPETERSON, K. J., SUMMONS, R. E., & DONOGHUE, P. C. J. (2007) · Palaeontology · doi:10.1111/j.1475-4983.2007.00692.x · Cited by 93
“Of course, molecular clocks are not without their problems (Rodriguez-Trelles et al. 2002; Smith and Peterson 2002; Benton and Ayala 2003; Bromham and Penny 2003; Donoghue and Smith 2003; Graur and Martin 2004; Roger and Hug 2006).”
BackgroundToward a syntactic phylogeny of modern Indo-European languages
Longobardi, G., Guardiano, C., Silvestri, G., Boattini, A., & Ceolin, A. (2013) · Journal of Historical Linguistics · doi:10.1075/jhl.3.1.07lon · Cited by 92
“…package, Felsenstein 1993), have the further property of producing 'ultrametric trees: i.e. trees complying with the 'molecular clock hypothesis' {Bromham & Penny 2003, Felsenstein 1993, 2004): in the rooted trees produced, the length of each branch, that is the distance between the root and…”
BackgroundLartillot, N., & Delsuc, F. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01558.x · Cited by 92
“Since then, such methods have been extensively used to establish the chronology of evolution in various phylogenetic groups (reviewed in Bromham and Penny 2003; Benton and Donoghue 2007).”
MethodPharmacophylogenomics: genes, evolution and drug targets
Searls, D. B. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1152 · Cited by 92
Battistuzzi, F. U., Filipski, A., Hedges, S. B., & Kumar, S. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq014 · Cited by 89
“Different clock methods may produce disparate times due to their implicit handling of the rate heterogeneity across lineages, the number and position of calibrations, and the set of genes analyzed (Bromham and Penny 2003; Ho and Larson 2006; Pulquerio and Nichols 2007).”
BackgroundRelaxed Molecular Clocks, the Bias–Variance Trade-off, and the Quality of Phylogenetic Inference
Wertheim, J. O., Sanderson, M. J., Worobey, M., & Bjork, A. C. (2009) · Systematic Biology · doi:10.1093/sysbio/syp072 · Cited by 87
“Despite its auspicious beginnings, however, the concept of a universal, strict molecular clock has fallen out of favor (Li 1993; Ayala 1997; Bromham and Penny 2003; Kumar 2005).”
BackgroundThe MiAge Calculator: a DNA methylation-based mitotic age calculator of human tissue types
Youn, A., & Wang, S. (2017) · Epigenetics · doi:10.1080/15592294.2017.1389361 · Cited by 82
“MiAge uses a molecular clock hypothesis [4].”
Rates of Mutation and Recombination in Siphoviridae Phage Genome Evolution over Three Decades
Kupczok, A., Neve, H., Huang, K. D., Hoeppner, M. P., Heller, K. J., Franz, C. M. A. P., & Dagan, T. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy027 · Cited by 85
“Homogeneous nucleotide substitution rates, which have been termed “molecular clock” (Zuckerkandl and Pauling 1965), are an important outcome of the neutral theory of molecular evolution (Kimura 1969; Bromham and Penny 2003).”
BackgroundKling, M. M., Mishler, B. D., Thornhill, A. H., Baldwin, B. G., & Ackerly, D. D. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0397 · Cited by 84
“…rates of molecular evolution vary among genes, rates for individual genes are often persistent within clades due to conserved characteristics such as genetic architecture and life-history traits [18–21], which suggests that molecular branch lengths may have utility in broadly predicting diversity.”
BackgroundPeng, Z., He, S., Wang, J., Wang, W., & Diogo, R. (2006) · Gene · doi:10.1016/j.gene.2005.11.024 · Cited by 85
“It should be stressed here, as by Bromham and Penny (2003), that lineage-specific variation in rate of molecular evolution can complicate molecular dating, because a calibration rate estimated from one lineage may not be an accurate representation of the rate in other lineages.”
BackgroundKessler, M. R. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511844898.003 · Cited by 83
Molecular clocks keep dispersal hypotheses afloat: evidence for trans‐Atlantic rafting by rodents
Rowe, D. L., Dunn, K. A., Adkins, R. M., & Honeycutt, R. L. (2009) · Journal of Biogeography · doi:10.1111/j.1365-2699.2009.02190.x · Cited by 82
“…inconsistencies have persisted despite the development of numerous and increasingly sophisticated methods of dealing with the inherent complexities of molecular-clock dating (Rodrı́guez-Trelles et al., 2002; Bromham & Penny, 2003; Bromham & Woolfit, 2004; Near & Sanderson, 2004; Rutschmann, 2006).”
Rasmussen, M. D., & Kellis, M. (2007) · Genome Research · doi:10.1101/gr.7105007 · Cited by 81
“function of the gene (Bromham and Penny 2003), and a species-specific substitution rate si dictated by the time interval and evolutionary dynamics of each lineage i (e.”
BackgroundInfluentialWang, Y., Liu, J., & Miehe, G. (2007) · Annals of Botany · doi:10.1093/aob/mcl259 · Cited by 82
“However, when palaeontological data are lacking, molecular estimates provide the only means of inferring the age of lineages (Li, 1997; Bromham and Penny, 2003).”
BackgroundArtificial Selection and Domestication: Modern Lessons from Darwin’s Enduring Analogy
Gregory, T. R. (2009) · Evolution Education and Outreach · doi:10.1007/s12052-008-0114-z · Cited by 89
“Moreover, because non-coding sequences usually are not constrained in the same manner as functional protein-coding genes, they are often thought to evolve largely at random and can be used (with caution) as “molecular clocks” to infer the timing of divergences among lineages (Bromham and Penny 2003; Ho and Larson 2006…”
BackgroundBayesian Molecular Clock Dating Using Genome-Scale Datasets
dos Reis, M., & Yang, Z. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9074-0_10 · Cited by 74
Zhang, D., Chen, M., Murphy, R. W., Che, J., Pang, J., Hu, J., Luo, J., Wu, S.-J., Ye, H., & Zhang, Y. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04747.x · Cited by 81
“In the absence of fossil or geological data, the molecular clock provides a valuable means of inferring the ages of lineage (Bromham & Penny 2003) yet such should be taken with caution.”
BackgroundMethodLi, Q., Qian, H., Shao, B., Hughes, R. P., & Aprahamian, I. (2018) · Journal of the American Chemical Society · doi:10.1021/jacs.8b07612 · Cited by 81
Sugui, J. A., Peterson, S. W., Abigail, F., Hansen, B. T., Samson, R. A., Mellado, E., Cuenca‐Estrella, M., & Kwon-Chung, K. J. (2014) · Journal of Clinical Microbiology · doi:10.1128/jcm.01704-14 · Cited by 80
“Routines were also run in Mega to determine whether these loci were suitable for determining evolutionary distance as a function of the molecular clock (20).”
MethodHogner, S., Laskemoen, T., Lifjeld, J. T., Porkert, J., Kleven, O., Albayrak, T., Kabasakal, B., & Johnsen, A. (2012) · Ecology and Evolution · doi:10.1002/ece3.398 · Cited by 80
“Hybridization is common in birds, occurring in approximately one out of 10 species (Grant and Grant 1992; McCarthy 2006).”
BackgroundSupport for vicariant origins of the New Zealand Onychophora
Allwood, J. S., Gleeson, D. M., Mayer, G., Daniels, S. R., Beggs, J. R., & Buckley, T. R. (2009) · Journal of Biogeography · doi:10.1111/j.1365-2699.2009.02233.x · Cited by 80
“…and testing hypotheses on vicariance Selecting a calibration point that matches the true age of lineage divergence is absolutely essential for obtaining accurate divergence time estimates (e.g. Thorne et al., 1998; Bromham & Penny, 2003; Heads, 2005; Ho et al., 2008; Ho & Phillips, 2009).”
BackgroundThe Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors
Baets, K. D., & Littlewood, D. T. J. (2015) · Advances in Parasitology/Advances in parasitology · doi:10.1016/bs.apar.2015.07.001 · Cited by 80
Using models of nucleotide evolution to build phylogenetic trees
Bos, D. H., & Posada, D. (2004) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2004.07.007 · Cited by 81
“Although the neutral theory has become pervasive in evolutionary genetics, the molecular clock does not always tick regularly [21].”
BackgroundMultiple host-switching of Haemosporidia parasites in bats
Duval, L., Robert, V., Csorba, G., Hassanin, A., Randrianarivelojosia, M., Walston, J., Nhim, T., Goodman, S., & Ariey, F. (2007) · Malaria Journal · doi:10.1186/1475-2875-6-157 · Cited by 78
“falciparum selection patterns [29].”
Biodiversity Conservation and Phylogenetic Systematics
Pellens, R., & Grandcolas, P. (2016) · Topics in biodiversity and conservation · doi:10.1007/978-3-319-22461-9 · Cited by 86
Molecular systematics: A synthesis of the common methods and the state of knowledge
Mauro, D. S., & Agorreta, A. (2010) · Cellular & Molecular Biology Letters · doi:10.2478/s11658-010-0010-8 · Cited by 80
“There is increasing evidence that the assumption of rate constancy is often violated, and that DNA and amino acid sequences of even closely related species can evolve at different rates [122, 123].”
BackgroundUse of phylogenetics in the molecular epidemiology and evolutionary studies of viral infections
Lam, T. T., Hon, C.-C., & Tang, J. W.-T. (2010) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408361003633318 · Cited by 83
“To correlate the temporal information, or their sampling dates, with their genetic differences, the concept of molecular clocks, which assume that substitutions accumulate over time at a roughly constant rate, has been applied.(56) Relying on this constant rate assumption, one can theoretically estimate the date of an…”
BackgroundSwart, B. L., Tolley, K. A., & Matthee, C. A. (2008) · Journal of Biogeography · doi:10.1111/j.1365-2699.2008.01988.x · Cited by 74
“Given the criticisms associated with using a constant molecular clock (Bromham & Penny, 2003; Kumar, 2005), we examined whether a constant mutation rate could reasonably be applied to the data set.”
Hipsley, C. A., Himmelmann, L., Metzler, D., & Müller, J. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-151 · Cited by 74
“This is commonly done by measuring the genetic distance between two species and, assuming mutations occur at a constant rate, applying an external calibration to convert those distances into geological time (for a review of molecular clock methods, see [2]).”
BackgroundZhang, J., Nie, Z., Wen, J., & Sun, H. (2011) · Taxon · doi:10.1002/tax.601003 · Cited by 73
Geological Dates and Molecular Rates: Rapid Divergence of Rivers and Their Biotas
Waters, J. M., Rowe, D. L., Apte, S., King, T. M., Wallis, G. P., Anderson, L., Norris, R. J., Craw, D., & Burridge, C. P. (2007) · Systematic Biology · doi:10.1080/10635150701313855 · Cited by 72
“Geologically based calibrations of molecular evolution provide an important method for formulating and testing evolutionary hypotheses and for understanding timeframes of biodiversifkation (Rambaut and Bromham, 1998; Bromham, 2003; Bromham and Penny, 2003; Sanmartin and Ronquist, 2004).”
MethodSchneeweiss, G. M. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01273.x · Cited by 70
“The situation is similar to that of a molecular clock in models of sequence evolution, which has been found to be violated in most of the real data sets (Bromham & Penny, 2003; Renner, 2005).”
MethodPoulin, É., GONZÁLEZ-WEVAR, C. A., Díaz, A., Gérard, K., & Hüne, M. (2014) · Global and Planetary Change · doi:10.1016/j.gloplacha.2014.07.017 · Cited by 70
“5 Jan time for a given lineage and therefore the genetic difference between any two species is proportional to the time since they last shared a common ancestor (Bromham and Penny, 2003).”
BackgroundEpimutations Define a Fast-Ticking Molecular Clock in Plants
Yao, N., Schmitz, R. J., & Johannes, F. M. (2021) · Trends in Genetics · doi:10.1016/j.tig.2021.04.010 · Cited by 69
Rutschmann, F., Eriksson, T., Schönenberger, J., & Conti, E. (2004) · International Journal of Plant Sciences · doi:10.1086/383335 · Cited by 69
“Additional theoretical and experimental studies of gene-specific effects on molecular dating estimates are clearly needed (Bromham and Penny 2003).”
BackgroundHuman Germline Mutation and the Erratic Evolutionary Clock
Moorjani, P., Gao, Z., & Przeworski, M. (2016) · PLoS Biology · doi:10.1371/journal.pbio.2000744 · Cited by 68
“One of the most fundamental discoveries in evolutionary biology is the “molecular clock”: the observation that changes to the genome along an evolutionary lineage accumulate steadily with time [1-3] and the subsequent development of a theory—the Neutral Theory—that explains why this behavior is expected for neutral ge…”
BackgroundEstimation of Mutation Rates and Coalescence Times: Some Caveats
Bandelt, H., Kong, Q., Richards, M. B., & Macaulay, V. A. (2006) · Springer eBooks · doi:10.1007/3-540-31789-9_4 · Cited by 68
Vicars, tramps and assembly of the New Zealand avifauna: a review of molecular phylogenetic evidence
Trewick, S. A., & Gibb, G. C. (2010) · Ibis · doi:10.1111/j.1474-919x.2010.01018.x · Cited by 65
Mathews, L. M., Adams, L., Anderson, E., Basile, M., Gottardi, E. A., & Buckholt, M. A. (2008) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2008.02.006 · Cited by 65
Vamathevan, J. J., Hall, M. D., Hasan, S., Woollard, P. M., Xu, M., Yang, Y., Li, X., Wang, X., Kenny, S., Brown, J. R., et al. (2013) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2013.04.007 · Cited by 65
“As expected, the murid clade had longer branches, which is explained by the body size hypothesis or the generation time hypothesis, which states that the larger the body size or the longer generation time is, the slower the molecular clock (Bromham and Penny, 2003).”
The Diversity Of Eukaryotes And The Root Of The Eukaryotic Tree
Brinkmann, H., & Philippe, H. (2008) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-74021-8_2 · Cited by 67
De Novo Mutation Rate Estimation in Wolves of Known Pedigree
Koch, E. M., Schweizer, R. M., Schweizer, T. M., Stahler, D. R., Smith, D. W., Wayne, R. K., & Novembre, J. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz159 · Cited by 66
Molecular phylogeny of the Notostraca
Korn, M., Rabet, N., Ghate, H. V., Marrone, F., & Hundsdoerfer, A. K. (2013) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2013.08.006 · Cited by 61
“…rates and longer effective generation times in these taxa, and hence it is probable that their rates of molecular evolution differ from those of other arthropods that lack such prolonged dormant stages (for a review of factors affecting rates of molecular evolution, see Bromham and Penny, 2003).”
BackgroundThe poplar pangenome provides insights into the evolutionary history of the genus
Zhang, B., Zhu, W., Diao, S., Wu, X., Lu, J., Ding, C., & Su, X. (2019) · Communications Biology · doi:10.1038/s42003-019-0474-7 · Cited by 64
Duchêne, D. A., Tong, K. J., Foster, C. S. P., Duchêne, S., Lanfear, R., & Ho, S. Y. W. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msz291 · Cited by 53
Carmi, O., Witt, C. C., Jaramillo, Á., & Dumbacher, J. P. (2016) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2016.05.029 · Cited by 64
“Given the many concerns that have been raised about potential pitfalls of divergence dating (e.g. Arbogast et al., 2002; Bromham and Penny, 2003; Ho et al., 2005), particularly in birds (e.g. Lavinia et al., 2016; Lovette, 2004; Nguyen and Ho, 2016), we present node ages as conditional hypotheses,…”
BackgroundAccelerated evolutionary rates in tropical and oceanic parmelioid lichens (Ascomycota)
Lumbsch, H. T., Hipp, A. L., Divakar, P. K., Blanco, O., & Crespo, A. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-257 · Cited by 61
“Background Differences in nucleotide substitution rates among taxa are a common phenomenon in molecular studies [1-7], and the presence of an exact molecular clock [8,9] appears to be a rare exception in molecular evolution, if present at all.”
BackgroundSamarakoon, M. C., Hyde, K. D., Hongsanan, S., McKenzie, E. H. C., Ariyawansa, H. A., Promputtha, I., Zeng, X., Tian, Q., & Liu, J. (2019) · Fungal Diversity · doi:10.1007/s13225-019-00423-8 · Cited by 61
“…fossil evidence in evolutionary studies is limited (Blair 2009), due to lack of sampling, uncertainty of the age, misleading phylogenetic classifications and incorrect calibrations (Marshall 1990; Bromham et al. 1999; Lee 1999; Bromham and Penny 2003; Near and Sanderson 2004; Parham et al. 2011).”
BackgroundThe genetic signature of recent speciation in manta rays (Manta alfredi and M. birostris).
Kashiwagi, T., Marshall, A., Bennett, M., & Ovenden, J. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.03.020 · Cited by 59
“Although the interpretation of molecular dating contains various caveats (Bromham, 2008; Bromham and Penny, 2003), the obtained tentative time intervals suggest that speciation and subsequent dispersal may have occurred during Pleistocene glacial cycles within 1 Ma (Hewitt, 1996, 2000; Hofreiter and Stewart, 2009; Jan…”
BackgroundAscomycota has a faster evolutionary rate and higher species diversity than Basidiomycota
Wang, H., Guo, S., Huang, M.-R., Thorsten, L. H., & Wei, J. (2010) · Science China Life Sciences · doi:10.1007/s11427-010-4063-8 · Cited by 61
Late Quaternary river drainage and fish evolution, Southland, New Zealand
Craw, D., Burridge, C. P., Anderson, L., & Waters, J. M. (2006) · Geomorphology · doi:10.1016/j.geomorph.2006.07.008 · Cited by 59
Identifying the confounding factors in resolving phylogenetic relationships in Vespertilionidae
Lack, J., & Bussche, R. A. V. D. (2010) · Journal of Mammalogy · doi:10.1644/09-mamm-a-354.1 · Cited by 59
“Since the initial suggestion of the constancy (with respect to time) of evolution by Zuckerkandl and Pauling (1962), a multitude of examples that violate the molecular clock hypothesis have been described (Bromham and Penny 2003).”
BackgroundFast Molecular Evolution Associated with High Active Metabolic Rates in Poison Frogs
Santos, J. C. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss069 · Cited by 58
“Likewise, the rate of the accumulation of nucleotide changes per unit of time also correlate with life history traits including physiological attributes at both organismal and cellular levels (Martin and Palumbi 1993; Bromham and Penny 2003; Gillooly et al. 2005).”
BackgroundHo, S. Y. W., & Lo, N. C. (2013) · Australian Journal of Entomology · doi:10.1111/aen.12018 · Cited by 57
Marshall, D. C., Hill, K. B. R., Moulds, M. S., Vanderpool, D., Cooley, J. R., Mohagan, A. B., & Simon, C. (2015) · Systematic Biology · doi:10.1093/sysbio/syv069 · Cited by 58
Effects of metabolic rate on protein evolution
Gillooly, J. F., McCoy, M. W., & Allen, A. P. (2007) · Biology Letters · doi:10.1098/rsbl.2007.0403 · Cited by 57
“Resolution of this issue has been hampered by our limited understanding of the factors that control mutation rates (Bromham & Penny 2003).”
BackgroundDeWoody, J. A. (2005) · Journal of Wildlife Management · doi:10.2193/0022-541x(2005)69[1400:mattso]2.0.co;2 · Cited by 57
“For example, neutral markers and their associated molecular clocks (Bromham and Penny 2003) can be used to determine how long ago human and chimpanzees lineages split from each other.”
BackgroundTectonic blocks and molecular clocks
Baets, K. D., Antonelli, A., & Donoghue, P. C. J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0098 · Cited by 55
“Thus, although the molecular clock has conventionally been employed in groups with a good fossil record to assess the efficacy of the fossil record, tectonic calibrations allow us to realize the original but forgotten aim of the molecular clock—to establish an evolutionary timescale for lineages lacking an appreciable…”
BackgroundAllegrucci, G., Todisco, V., & Sbordoni, V. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.04.022 · Cited by 55
Bontell, I., Hall, N., Ashelford, K. E., Dubey, J. P., Boyle, J. P., Lindh, J. G., & Smith, J. E. (2009) · Genome biology · doi:10.1186/gb-2009-10-5-r53 · Cited by 55
“Divergence time estimates rely on the assumption that the mutation rate in a species remains relatively constant over time [39,40].”
BackgroundMolecular and Paleontological Evidence for a Post-Cretaceous Origin of Rodents
Wu, S., Wu, W.-Y., Zhang, F., Ye, J., Ni, X., Sun, J., Edwards, S. V., Meng, J., & Organ, C. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046445 · Cited by 60
“These estimates are broadly consistent with the paleontological record, but challenge previous molecular studies that place the origin and early diversification of rodents in the Cretaceous.”
BackgroundResultInfluentialTinn, O., & Oakley, T. H. (2008) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2008.03.001 · Cited by 54
Evolution of Xylariomycetidae (Ascomycota: Sordariomycetes)
Samarakoon, M. C. (2016) · Mycosphere · doi:10.5943/mycosphere/7/11/9 · Cited by 54
“Speciation events can provide valuable information concerning the genetic evolution and evolutionary history of taxon groups, through biochemical, selective pressure and population processes (Bromham & Penny 2003).”
BackgroundFast Genes and Slow Clades: Comparative Rates of Molecular Evolution in Mammals
Bininda‐Emonds, O. R. P. (2007) · Evolutionary Bioinformatics · doi:10.1177/117693430700300008 · Cited by 56
“…rate than nDNA, on average, because the mitochondrion is both the source of oxidative phosphorylation in animals (with an increased mutagen production as by-products of metabolic processes) and uses a DNA polymerase-γ with its higher error rate for DNA replication (Bromham and Penny, 2003).”
BackgroundInfluentialMolecular dates for the “cambrian explosion”: The influence of prior assumptions.
Welch, J. J., Fontanillas, E., & Bromham, L. (2005) · Systematic Biology · doi:10.1080/10635150590947212 · Cited by 53
“There is now a great deal of evidence suggesting that rates of molecular evolution may vary substantially between lineages (e.g., Bromham and Penny, 2003 ).”
BackgroundSelf-citationDid dung beetles arise in Africa? A phylogenetic hypothesis based on five gene regions
Sole, C. L., & Scholtz, C. H. (2010) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2010.04.023 · Cited by 53
Pascual‐García, A., Abia, D., Méndez, R., Nido, G. S., & Bastolla, U. (2009) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.22616 · Cited by 51
Counting Divisions in a Human Somatic Cell Tree: How, What and Why
Shibata, D. K., & Tavaré, S. (2006) · Cell Cycle · doi:10.4161/cc.5.6.2570 · Cited by 53
How can we determine the molecular clock of malaria parasites?
Bensch, S., Hellgren, O., Križanauskienė, A., Palinauskas, V., Valkiūnas, G., Outlaw, D. C., & Ricklefs, R. E. (2013) · Trends in Parasitology · doi:10.1016/j.pt.2013.03.011 · Cited by 53
Inferring human stem cell behaviour from epigenetic drift
Shibata, D. K. (2008) · The Journal of Pathology · doi:10.1002/path.2461 · Cited by 53
“Analysing genome variation is difficult because a simple molecular clock hypothesis is incorrect and many aspects of molecular phylogeny are controversial [1,29].”
Building trees of algae: some advances in phylogenetic and evolutionary analysis
Verbruggen, H., & Theriot, E. C. (2008) · European Journal of Phycology · doi:10.1080/09670260802207530 · Cited by 53
Unifying Vertical and Nonvertical Evolution: A Stochastic ARG-based Framework
Bloomquist, E. W., & Suchard, M. A. (2009) · Systematic Biology · doi:10.1093/sysbio/syp076 · Cited by 50
“Over the past decade, investigators have realized the shortcomings of a strict molecular clock (Zuckerkandl and Pauling 1965; Bromham and Penny 2003) and have introduced several models to relax this assumption for bifurcating trees (Thorne et al. 1998; Aris-Brosou and Yang 2002; Drummond et al.…”
BackgroundZhang, Z., Zhao, P., & Cai, L. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01407 · Cited by 50
“Molecular clock hypothesis is useful in estimating divergence times (Boutin and Coineau, 2000; Bromham and Penny, 2003).”
Backgroundde la Paz, J. A., Nartey, C. M., Yuvaraj, M., & Morcos, F. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913071117 · Cited by 50
“The Neutral Theory of Evolution has been a successful assumption that accounts for the relative constancy of the substitution rate observed in the molecular clock as well as how allele diversity is produced by genetic drift (5–7).”
Seeing the Tree of Life behind the phylogenetic forest
Puigbò, P., Wolf, Y. I., & Koonin, E. V. (2013) · BMC Biology · doi:10.1186/1741-7007-11-46 · Cited by 49
“Having established the validity of the STOL, we employed it to reassess a fundamental aspect of evolutionary theory, the molecular clock (MC) model under which genes evolve at approximately constant genespecific rates [23].”
MethodAllen, B., Sample, C., Dementieva, Y. A., Medeiros, R. C., Paoletti, C., & Nowak, M. A. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004108 · Cited by 48
“A number of factors can alter the rate of neutral substitution [3, 4], including selection, changes in population demography over time, or mutation rates that vary systematically by demographic classes [5, 6] or sex [7].”
BackgroundBayesian phylogenetic estimation of fossil ages
Drummond, A. J., & Stadler, T. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0129 · Cited by 46
“Although there has indeed been much controversy surrounding apparent discrepancies between palaeontological and molecular phylogenetic inferences [2], it is also clear that fossil and molecular data both produce broadly concordant views of evolutionary history [3].”
BackgroundABRUPT DECELERATION OF MOLECULAR EVOLUTION LINKED TO THE ORIGIN OF ARBORESCENCE IN FERNS
Korall, P., Schuettpelz, E., & Pryer, K. M. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01000.x · Cited by 48
Wilson, M. V. H., & Murray, A. M. (2008) · Geological Society London Special Publications · doi:10.1144/sp295.12 · Cited by 48
“However, rates of mutation or ‘molecular evolution’ may vary greatly among different taxa (Bromham & Penny 2003), and may also vary over time within a lineage (e.g. Ruber & Zardoya 2005).”
BackgroundUniversal Pacemaker of Genome Evolution
Snir, S., Wolf, Y. I., & Koonin, E. V. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002785 · Cited by 46
Metadata
- Authors
- Bromham, L., & Penny, D.
- Affiliations
- University of Sussex (GB)
- Allan Wilson Centre (NZ)
- Corresponding author
- Bromham, Lindell
- ORCID
- Bromham, Lindell
- Venue
- Nature Reviews Genetics
- Published
- 2003-03
- Volume
- 4
- Issue
- 3
- Pages
- 216-224
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2062220010
- Semantic Scholar
- 07e298aa4bc7299c0bfd8164d900b90ce80102a2
- Cited by
- 615
- References
- 74
- Citations by year
- 2026: 9 · 2025: 15 · 2024: 17 · 2023: 14 · 2022: 11 · 2021: 25 · 2020: 21 · 2019: 21 · 2018: 17 · 2017: 20 · 2016: 27 · 2015: 24 · 2014: 50 · 2013: 40 · 2012: 27
- FWCI
- 3.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Figshare (submittedVersion)
- ANU Open Research (Australian National University) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- molecular clock, molecular evolution rate, neutral theory of molecular evolution, rate variation, divergence time estimation, evolutionary history, viral epidemics
- MeSH terms
- Animals, Disease Outbreaks, DNA, Genetics, Population, Humans, Models, Genetic, Mutation, Population Density, Proteins, Selection, Genetic, Time Factors, Evolution, Molecular, Communicable Diseases, Emerging, History, Ancient
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