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Rates of Nucleotide Substitution in Primates and Rodents and the Generation–Time Effect Hypothesis
Abstract
DNA sequence data from introns, flanking regions, and the eta globin pseudogene region all show a significantly higher rate of nucleotide substitution in the Old World monkey lineage than in the human lineage after the separation of the two lineages, or, in other words, the data support the hominoid rate-slowdown hypothesis. Data from both protein sequences and DNA sequences show that the rate of evolution is significantly higher in the rodent lineage than in the primate lineage. Furthermore, DNA sequences from introns show that the rate of nucleotide substitution is at least two times higher in rodents than in higher primates. The male-to-female ratio of mutation rate is estimated to be between 3 and 6 in higher primates, whereas it is only 2 in mice and rats. These ratios are similar to the corresponding male-to-female ratios of germ cell divisions in higher primates and in rodents, suggesting that errors in DNA replication during germ cell division are the primary source of mutation, or, in other words, mutation is largely DNA replication-dependent. This conclusion provides further support for the generation-time effect hypothesis.
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“For example, the substitution rate in murid rodents is, on average, two to three times faster than the rate in hominid primates (apes and humans) 32 .”
From The modern molecular clock (2003) · cites this paper as [32]
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“For this estimate, we assumed that neutral substitution biases were similar in rodent and primate evolution and that the average substitution level since the rodent–primate split is 18% in human DNA and 35% in mouse DNA (Li et al. 1996).”
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“For example, rodents are known to have an elevated rate of substitution, compared to most of the mammals (Li et al., 1996; Weinreich, 2001).”
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“Notably, the textbook view that replication errors are the primary source of human mutations (Drost and Lee, 1995; Li et al., 1996; Crow, 2000; Strachan and Read, 2010) often invokes the increase in the number of germline mutations with paternal age (Crow, 2000; Drost & Lee, 1995).”
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“The generation time hypothesis suggests that species with shorter generation times (e.g. herbaceous plants) accumulate more replication errors per unit time because they copy their genomes more often, which results in higher mutation rates (Li et al. 1996).”
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“Considering the SNPs as defining background haplotypes (upon which STRP alleles are found) and considering estimates for mutation rates for single nucleotides on the order of 10 ‐8 (Crow 1995; Li et al. 1996 ), we conclude that the B2-D2-A1 background haplotype (ignoring the STRP) is the ancestral hominid haplotype, a…”
BackgroundMolecular Clocks and Nucleotide Substitution Rates in Higher Plants
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Sensitivity of the relative-rate test to taxonomic sampling
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“There are two hypotheses that might explain these differences in DNA substitution rates: the generation time effect hypothesis (Li et al. 1996); and the metabolic rate hypothesis (Martin 1995).”
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“Additional information on protein-protein interactions (De et al. 2009, Lin et al. 2011) and biochemical networks will also be useful, because it is plausible that evolutionary rates are a function of protein connectivity and network position.”
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“With mutation rates for single nucleotides estimated at ∼1028 (Crow 1995; Li et al. 1996), any SNP must represent effectively a single mutational event that has reached polymorphic frequencies through random genetic drift (or selection or hitchhiking).”
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“This estimate might be low for rodents, given their accelerated rate of molecular evolution (Martin & Palumbi 1993; Li et al. 1996; Triant & DeWoody 2006).”
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“These observations have been taken both as evidence for the view that mutations occur mainly during DNA replication in the germ line and as support for the generation-time effect hypothesis 90 , which postulates that the molecular clock runs faster in short-living animals than in long-living ones.”
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Interpreting the Dependence of Mutation Rates on Age and Time
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“An example of such data sets is mammalian data where the rodent lineages have accelerated rates of substitution (Wu and Li 1985; Britten 1986; Martin and Palumbi 1993; Li et al. 1996).”
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“The original explanation for this rate heterogeneity is that species with shorter generation times have a greater number of DNA replications per year, thus incurring an increased chance of replication error per unit time (Li, Tanimura, and Sharp 1987; Ohta 1993; Mooers and Harvey 1994; Li et al. 1996).”
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High and Variable Rates of Repeat-Mediated Mitochondrial Genome Rearrangement in a Genus of Plants
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Vagaries of the molecular clock.
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Low Levels of Nucleotide Diversity in Mammalian Y Chromosomes
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“The extent of the male bias is likely to be positively correlated with generation time (Chang et al. 1994; Li et al. 1996; Bartosch-Härlid et al. 2003), and available data would thus suggest that mammalian am ranges approximately from 2 (short-lived species like most rodents) to 5 (humans).”
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“Smaller, shorter-lived mammals with high metabolic rates and short germ-line generation times accumulate mutations at a higher rate (Li et al. 1996).”
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“Although the generation time of Muridae is much shorter than that of Hominidae (Li et al. 1996), this difference alone cannot fullyexplain the difference between evolutionary rates that we observe.”
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Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements
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BackgroundComparative analysis of phylogenetic and fishing effects in life history patterns of teleost fishes
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“This might partially be explained by differences in generation times between the different species (81, 100), although the magnitude of this effect is debated (75).”
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Variable molecular clocks in hominoids
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LIFE HISTORY AND THE MALE MUTATION BIAS
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“Notable examples include the hominoid rateslow-down hypothesis (Li et al. 1996), which is consistent with an effect of generation time, the negative correlation between body size and rate of molecular evolution seen in a variety of taxa (Martin and Palumbi 1993a; Bromham 2002) and the slower rate…”
BackgroundResultGenomic analysis of orthologous mouse and human olfactory receptor loci
Lane, R. P., Cutforth, T., Young, J. M., Athanasiou, M., Friedman, C. L., Rowen, L., Evans, G. A., Axel, R., Hood, L., & Trask, B. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.131215398 · Cited by 98
Lercher, M. J., Williams, E. J. B., & Hurst, L. D. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003744 · Cited by 97
“Just this method has been applied for flies (Bauer and Aquadro 1997), rodents (Chang et al. 1994; Chang and Li 1995; Li et al. 1996; McVean and Hurst 1997; Smith and Hurst 1999a), cats (Slattery and O’Brien 1998), birds (Ellegren and Fridolfsson 1997), and primates (Shimmin, Chang, and Li 1993,…”
BackgroundMethodEvolution of genes and taxa: a primer
Doyle, J. J., & Gaut, B. S. (2000) · Plant Molecular Biology · doi:10.1023/a:1006349518932 · Cited by 95
“The extent to which either the time-calibrated clock or the generation-time clock holds is unclear, despite extensive empirical efforts [149, 82, 23, 83].”
BackgroundMcGowen, M. R., Grossman, L. I., & Wildman, D. E. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.0869 · Cited by 100
Heterogeneous Genomic Molecular Clocks in Primates
Kim, S., Elango, N., Warden, C., Vigoda, E., & Yi, S. V. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0020163 · Cited by 95
“consequence of the difference in generation times, evolutionary rates of replication-dependent substitutions are slower in hominoids than in Old World monkeys [2,4,25].”
BackgroundKAYANG, B. B., Fillon, V., Inoue‐Murayama, M., Miwa, M., Leroux, S., Fève, K., Monvoisin, J. L., Frédérique Pitel, A., Vignoles, M., Mouilhayrat, C., et al. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-101 · Cited by 96
“Similar times of divergence can be found between humans and New World monkeys (35 million years) or humans and Old World monkeys (30 million years) [31], for which numerous interchromosomal events have been documented [32,33].”
BackgroundTomasco, I. H., & Lessa, E. P. (2011) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.06.014 · Cited by 95
“…allow us to reject alternative, non-selectionist explanations of rate variation, such as a relaxation of purifying selection, variation in metabolic rate, body mass, population size, and generation time among lineages (Bromham et al., 1996; Li et al., 1996; Martin, 1995; Martin and Palumbi, 1993).”
BackgroundLartillot, N., & Delsuc, F. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01558.x · Cited by 92
PHYLOGEOGRAPHY OF THE PLANKTONIC CHAETOGNATH SAGITTA SETOSA REVEALS ISOLATION IN EUROPEAN SEAS
Peijnenburg, K. T. C. A., Breeuwer, J. A. J., Pierrot-Bults, A. C., & Menken, S. B. J. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01728.x · Cited by 92
Insights from human/mouse genome comparisons
Pennacchio, L. A. (2003) · Mammalian Genome · doi:10.1007/s00335-002-4001-1 · Cited by 86
“While it remains unclear why this has occurred, one possible explanation is the shorter generation time and consequent increased amount of selection in mice relative to humans (Li et al. 1996).”
BackgroundComparative analysis of protein coding sequences from human, mouse and the domesticated pig
Jørgensen, F. G., Hobolth, A., Hornshøj, H., Bendixen, C., Fredholm, M., & Schierup, M. H. (2005) · BMC Biology · doi:10.1186/1741-7007-3-2 · Cited by 84
“For a more thorough discussion of the generation time hypothesis in mammals see [43].”
Genetic structure of fragmented populations of red squirrel (Sciurus vulgaris) in the UK
Barratt, E. M., Gurnell, J., Malarky, G., Deaville, R. C., & Bruford, M. W. (1999) · Molecular Ecology · doi:10.1046/j.1365-294x.1999.00771.x · Cited by 85
The Mouse Lemur, a Genetic Model Organism for Primate Biology, Behavior, and Health
Ezran, C., Karanewsky, C. J., Pendleton, J. L., Sholtz, A., Biermann, M. R., Willick, J., Razafindrakoto, A., Zohdy, S., Albertelli, M. A., & Krasnow, M. A. (2017) · Genetics · doi:10.1534/genetics.116.199448 · Cited by 78
Why does dosage compensation differ between XY and ZW taxa?
Naurin, S., Hansson, B., Bensch, S., & Hasselquist, D. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.11.006 · Cited by 79
Metadata
- Authors
- Li, W.-H., Ellsworth, D. L., Krushkal, J., Chang, B. H.-J., & Hewett-Emmett, D.
- Affiliations
- The University of Texas Health Science Center at Houston (US)
- Venue
- Molecular Phylogenetics and Evolution
- Publisher
- Elsevier BV
- Published
- 1996-02
- Volume
- 5
- Issue
- 1
- Pages
- 182-187
- ISSN
- 1055-7903 (ISSN-L)
- OpenAlex
- W2068919087
- Cited by
- 335
- References
- 0
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 3 · 2023: 8 · 2022: 10 · 2021: 6 · 2020: 4 · 2019: 5 · 2018: 11 · 2017: 11 · 2016: 9 · 2015: 6 · 2014: 9 · 2013: 17 · 2012: 9
- FWCI
- 10.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Phylogenetics and Evolution (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- nucleotide substitution rates, Old World monkeys, hominoid evolution, rodent evolution, primate evolution, introns, DNA replication errors, mutation rate
- MeSH terms
- Animals, DNA, Female, Globins, Humans, Introns, Male, Models, Genetic, Mutation, Primates, Pseudogenes, Rodentia, Sex Chromosomes, Time Factors, Hominidae, Evolution, Molecular, Mice, Rats
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