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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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“Evidence for the generation time effect has come from studies on various proteins and species including analyses of substitution rates in higher primates and rodents [5], substitution rates in higher grasses and in palms [6], in mammalian genomes [7] and in chloroplast and sex mutation rate ratios [5,6].”
Correlation Between the Substitution Rate and Rate Variation Among Sites in Protein Evolution
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“In most of these cases, the primer was designed to exactly match the human gene sequence because it is thought that primate molecular evolution is significantly slower than rodent evolution and the human should, therefore, be more likely to match the sequence of the common ancestor to primates and rodents [34].”
BackgroundGenomics and Clinical Medicine: Rationale for Creating and Effectively Evaluating Animal Models
Swanson, K. S., Mazur, M. J., Vashisht, K., Rund, L. A., Beever, J. E., Counter, C. M., & Schook, L. B. (2004) · Experimental Biology and Medicine · doi:10.1177/153537020422900902 · Cited by 48
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Kondrashov, A. S. (1998) · Genetica · doi:10.1023/a:1017085731998 · Cited by 45
“Comparisons of mouse and rat sequences suggest a similar (Wolfe & Sharp, 1993; Li et al., 1996).”
BackgroundRands, C. M., Darling, A. E., Fujita, M. K., Kong, L., Webster, M. T., Clabaut, C., Emes, R. D., Heger, A., Meader, S., Hawkins, M. B., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-95 · Cited by 50
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BackgroundYang, Y.-F., Zhu, T., & Niu, D. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt043 · Cited by 50
“In both plants and animals, many previous studies have shown that organisms with short generations have higher substitution rates than organisms with longer generations (Gaut et al. 1996, 2011; Li et al. 1996; Nikolaev et al. 2007; Soria-Hernanz et al. 2008; Muller and Albach 2010).”
ResultHigh variability and non-neutral evolution of the mammalian avpr1a gene
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Generation time, life history and the substitution rate of neutral mutations
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“The result is an LBA effect derived from having a mixture of long and short germ line generation times in the dataset, where the species with a short germ line generation time assumes a basal position in the phylogeny [26] [27] [28].”
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Hoffman, M. M., & Birney, E. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl179 · Cited by 42
“Although the human–murid divergence occurred later (85–88 MYA) (Springer et al. 2003), the human–murid evolutionary distance is longer than the distance between human and dog, probably partly due to shorter generation time in the murid lineage (Li et al. 1996).”
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“Although controversial (cf. Easteal & Herbert, 1997; Li et al., 1996; Li, Gouy, Sharp, O’hUigin, & Yang, 1990), comparative studies suggest that the substitution rate of rodents might be two to four times faster than that of humans, differences that accelerated more recently in time after these lineages diverged from…”
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“…reports on the correlation between the rate of nucleotide substitution and various factors such as body mass (as reviewed in Martin and Palumbi 1993), body size and temperature (Gillooly et al. 2005), metabolic rate (Martin 1995), and generation time (Li et al. 1996; Lehtonen and Lanfear 2014).”
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“The genomes of rodents change faster than those of primates [31,39-41].”
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Galtier, N., & Mouchiroud, D. (1998) · Genetics · doi:10.1093/genetics/150.4.1577 · Cited by 41
What can DNA Tell us About the Cambrian Explosion?
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(Why) Does Evolution Favour Embryogenesis?
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A comparative study on karyotypic diversification rate in mammals
Martínez, P. A., Jacobina, U. P., Fernandes, R. V., Bessa-Brito, C. D., Penone, C., Amado, T. F., Fonseca, C. R., & Bidau, C. J. (2016) · Heredity · doi:10.1038/hdy.2016.110 · Cited by 35
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Molecular clock or erratic evolution? A tale of two genes.
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“The best-documented case of a generation time effect is the 2- to 3-fold faster substitution rate in rodents compared to hominids [12,7].”
BackgroundLinde, A., Eklund, D. M., Cronberg, N., et al. (2021) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2021.107295 · Cited by 32
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“Some examples of such traits include metabolic rate (Martin and Palumbi 1993; Bleiweiss 1998), longevity (Nabholz et al. 2008), population size (Lynch 2010), and generation time (Li et al. 1996).”
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“For example, although rates of substitution vary from protein to protein, rodents consistently replace amino acids at a higher rate than do primates (Li et al. 1996).”
BackgroundSelf-citationNeutralism and selectionism: the molecular clock
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“The generation-time hypothesis (Wu and Li, 1985; Gaut et al., 1992; Li et al., 1996) cannot account for the erratic patterns of GPDH and SOD.”
BackgroundEvolution of the Couple Cytochrome c and Cytochrome c Oxidase in Primates
Pierron, D., Wildman, D. E., Hüttemann, M., Letellier, T., & Grossman, L. I. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3573-0_8 · Cited by 30
“be predicted from either their rate during previous mammalian descent or by the slowdown in the mutation rate in primates (Wu and Li, 1985; Bailey et al., 1991; Li et al., 1996).”
BackgroundInfluentialThrough a Glass, Darkly: Reflections of Mutation From lacI Transgenic Mice
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“For example, rodents have a faster substitution rate than primates (3, 4), and hominoids have a slower rate of molecular evolution than other primates, a phenomenon called the ‘‘hominoid slowdown’’ (5–10).”
BackgroundHeterogeneous Tempo and Mode of Conserved Noncoding Sequence Evolution among Four Mammalian Orders
Babarinde, I. A., & Saitou, N. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt177 · Cited by 30
“Rodents have a significantly high percent difference and primates have the lowest percent difference (t-test P<10 180), consistent with Li et al. (1996) and several other studies that rodents have higher substitution rates.”
ResultMapping and monitoring bird populations: their conservation uses
Underhill, L. G., & GIBBONS, D. W. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606304.004 · Cited by 27
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Lane, R. P., Roach, J. C., Lee, I. Y., Boysen, C., Smit, A. F. A., Trask, B. J., & Hood, L. (2002) · Genome Research · doi:10.1101/gr.197901 · Cited by 27
“This coding sequence similarity is remarkable given the twofold difference in estimated molecular clock rates for these species (Li et al. 1996).”
On the association between chromosomal rearrangements and genic evolution in humans and chimpanzees
Marquès‐Bonet, T., Sànchez-Ruiz, J., Armengol, L., Khaja, R., Bertranpetit, J., López-Bigas, N., Rocchi, M., Gazave, É., & Navarro, A. (2007) · Genome biology · doi:10.1186/gb-2007-8-10-r230 · Cited by 26
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“This is supported by the generation time effect hypothesis, which states that the shorter the generation time, the more mutations can be passed on in a fixed amount of time, thus increasing the evolutionary rate (Li et al. 1996).”
BackgroundTracing the Origin of HLA-DRB1 Alleles by Microsatellite Polymorphism
Bergström, T. F., Engkvist, H., Erlandsson, R., et al. (1999) · The American Journal of Human Genetics · doi:10.1086/302401 · Cited by 26
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“The generation-time hypothesis predicts faster nucleotide substitution rates per unit time in species with shorter generation times, as DNA replication errors (probably during stem cell division) accumulate more often per absolute time (e.g. Laird et al. 1969; Li et al. 1996).”
BackgroundEastern Beringian biogeography: historical and spatial genetic structure of singing voles in Alaska
Weksler, M., Lanier, H. C., & Olson, L. E. (2010) · Journal of Biogeography · doi:10.1111/j.1365-2699.2010.02310.x · Cited by 24
“103 substitutions site Myr) encompasses the mitochondrial silent substitution rate estimated for mammals (Brown et al., 1979, 1982; Irwin et al., 1991; Li et al., 1996) and is in accordance with values used in studies of other rodents (Arbogast, 1999; Arbogast et al.”
ResultWang, H., Ding, K., Zhang, Y., Li, J., Kullo, I. J., & He, F. (2007) · Pharmacogenetics and Genomics · doi:10.1097/fpc.0b013e328165249f · Cited by 25
Zee, J. P. V., Schlueter, J. A., Schlueter, S. D., et al. (2016) · BMC Genomics · doi:10.1186/s12864-015-2350-2 · Cited by 23
“Consequently, synonymous substitution rates (Ks values) are often used to formulate molecular clock estimates [25, 26].”
MethodGenomic Background and Generation Time Influence Deleterious Mutation Rates in Daphnia
Latta, L. C., Morgan, K., Weaver, C. S., Allen, D. E., Schaack, S., & Lynch, M. (2012) · Genetics · doi:10.1534/genetics.112.146571 · Cited by 23
“An effect of generation time may be largely due to the increase in germline cell divisions occurring in older parents, which result in additional opportunities for DNA replication error (Li et al. 1996; Drake et al. 1998).”
BackgroundAn empirical estimate of the generation time of mouse lemurs
Radespiel, U., Lutermann, H., Schmelting, B., & Zimmermann, E. (2019) · American Journal of Primatology · doi:10.1002/ajp.23062 · Cited by 20
Janečka, J. E., Chowdhary, B. P., & Murphy, W. J. (2012) · Journal of Biosciences · doi:10.1007/s12038-012-9254-y · Cited by 22
“For example, humans have a greater number of germline cell divisions than mice, and therefore their substitution rate is not as low relative to mice as would be predicted from just generation time (Li et al. 1996; Bromham 2011).”
BackgroundInfluentialGlobal Rate Variation in Bony Vertebrates
Takezaki, N. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy125 · Cited by 21
Ma, C., YeYing, W., Wu, C., Kang, L., & Liu, C.-X. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1156 · Cited by 22
“In addition, metabolic rate, generation time, and environmental temperature are also correlated with substitution rate variations [73,74].”
Evolution ofRattus(mammalia, Rodentia) during the plio‐pleistocene in Thailand
Chaimanee, Y., & Jaeger, J. (2001) · Historical Biology · doi:10.1080/10292380109380590 · Cited by 21
Mosaic genealogy of the Mus musculus genome revealed by 21 nuclear genes from its three subspecies
Liu, Y., Takahashi, A., Kitano, T., Koide, T., Shiroishi, T., Moriwaki, K., & Saitou, N. (2008) · Genes & Genetic Systems · doi:10.1266/ggs.83.77 · Cited by 21
Lecointe, N., Meerabux, J., Ebihara, M., et al. (1999) · Oncogene · doi:10.1038/sj.onc.1202645 · Cited by 21
“Analysis of a GenBank cosmid (U73638) which covers the 3' end of the LPC gene, revealed the presence of the gene SM22, which encodes a calponin-related protein, speci®cally expressed in adult smooth muscle (Li et al., 1996a).”
BackgroundInfluentialWidespread Ultraconservation Divergence in Primates
Ovcharenko, I. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn116 · Cited by 21
“Evolutionary sequence conservation is a reliable indicator of biological function in the analysis of anonymous sequences of genomes (Loots et al. 2000; Dermitzakis et al. 2003; Woolfe et al. 2005).”
Hernández‐Andreu, J. M., Giner, P., & Hernández-Yago, J. (1999) · Gene · doi:10.1016/s0378-1119(99)00409-6 · Cited by 21
Priority-setting in species conservation
Mace, G. M., & Collar, N. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606304.005 · Cited by 21
De novo mutations in children born after medical assisted reproduction
Smits, R., Xavier, M. J., Oud, M. S., Astuti, G., Meijerink, A. M., de Vries, P. F., Holt, G. S., Alobaidi, B., Batty, L. E., Khazeeva, G., et al. (2022) · Human Reproduction · doi:10.1093/humrep/deac068 · Cited by 22
Superoxide dismutase 1 is positively selected to minimize protein aggregation in great apes
Dasmeh, P., & Kepp, K. P. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2519-8 · Cited by 17
“Multiple regression supported metabolic rate as more explanatory of the evolutionary rate [81], whereas male–female evolutionary rate comparisons in rodents and primates supported a major role of generation time [76].”
BackgroundResultInfluentialAccelerated evolution of an Lhx2 enhancer shapes mammalian social hierarchies
Wang, Y., Dai, G., Gu, Z., Liu, G., Tang, K., Pan, Y.-H., Chen, Y., Lin, X., Wu, N., Chen, H.-S., et al. (2020) · Cell Research · doi:10.1038/s41422-020-0308-7 · Cited by 21
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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