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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The substitution rate in murid rodents is, on average, two to three times faster than the rate in hominid primates (apes and humans).
“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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International Human Genome Sequencing Consortium, Whitehead Institute for Biomedical Research, C. F. G. R., Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., et al. (2001) · Nature · doi:10.1038/35057062 · Cited by 24,216 · see citing works
Initial sequencing and comparative analysis of the mouse genome
Mouse Genome Sequencing Consortium (2002) · Nature · doi:10.1038/nature01262 · Cited by 7,187 · see citing works
The evolution of gene expression levels in mammalian organs
Brawand, D., Soumillon, M., Necsulea, A., Julien, P., Csárdi, G., Harrigan, P., Weier, M., Liechti, A., Aximu-Petri, A., Kircher, M., et al. (2011) · Nature · doi:10.1038/nature10532 · Cited by 1,248 · see citing works
Brookes, A. J. (1999) · Gene · doi:10.1016/s0378-1119(99)00219-x · Cited by 1,381 · see citing works
PipMaker—A Web Server for Aligning Two Genomic DNA SequencesPreprint
Schwartz, S., Zhang, Z., Frazer, K. A., Smit, A. F. A., Riemer, C., Bouck, J. B., Gibbs, R. A., Hardison, R. C., & Miller, W. (2000) · Genome Research · doi:10.1101/gr.10.4.577 · Cited by 1,165 · see citing works
“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).”
BackgroundInfluentialGaut, B. S., Morton, B. R., McCaig, B. C., & Clegg, M. T. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.19.10274 · Cited by 773 · see citing works
Positive Darwinian selection after gene duplication in primate ribonuclease genes
Zhang, J., Rosenberg, H. F., & Nei, M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3708 · Cited by 736 · see citing works
Comparative analyses of multi-species sequences from targeted genomic regions
Thomas, J. W., Touchman, J., Blakesley, R. W., Bouffard, G. G., Beckstrom‐Sternberg, S. M., Margulies, E. H., Blanchette, M., Siepel, A. C., Thomas, P. J., McDowell, J. C., et al. (2003) · Nature · doi:10.1038/nature01858 · Cited by 630 · see citing works
“Our findings confirm that the genomes of rodents are changing faster than those of primates, carnivores and artiodactyls, in agreement with many report”
ResultBromham, L., & Penny, D. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1020 · Cited by 615 · see citing works
“and this is consistent with the higher rate of molecular evolution in murid rodents than in hominid”
ResultMutation rates in mammalian genomes
Kumar, S., & Subramanian, S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.022629899 · Cited by 584 · see citing works
Nucleotide Substitution Rate of Mammalian Mitochondrial Genomes
Pesole, G., Gissi, C., Chirico, A. D., & Saccone, C. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006487 · Cited by 486 · see citing works
“A lineage-specific rate variation has been frequently explained by a generation time (Li et al. 1996; Li et al. 1987; Ohta 1993) or a metabolic rate (Martin et al.”
BackgroundRaaum, R. L., Sterner, K. N., Noviello, C., Stewart, C.-B., & Disotell, T. R. (2005) · Journal of Human Evolution · doi:10.1016/j.jhevol.2004.11.007 · Cited by 377 · see citing works
“…the relatively modest difference in mutation rate between hominoid and cercopithecoid nDNAd about 1.4-fold, the so-called ‘‘hominoid slowdown’’ (Goodman, 1961; Goodman et al., 1971; Li and Tanimura, 1987; Li et al., 1996)dhas been better accommodated by some authors (e.g., Goodman et al., 1998).”
BackgroundInfluentialPrimate molecular divergence dates
Steiper, M. E., & Young, N. M. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2006.05.021 · Cited by 336 · see citing works
“Support for the ‘hominoid slowdown’ has been oVered by many studies (Bailey et al., 1991; Elango et al., 2006; Ellsworth et al., 1993; Goodman, 1961; Goodman et al., 1971; Koop et al., 1986; Li and Tanimura, 1987; Li et al., 1987, 1996; Seino et al., 1992; Steiper et al., 2004; Yi et al., 2002).”
BackgroundNei, M., Xu, P., & Glazko, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051611498 · Cited by 329 · see citing works
Profiling Phylogenetic Informativeness
Townsend, J. P. (2007) · Systematic Biology · doi:10.1080/10635150701311362 · Cited by 332 · see citing works
“For example, rodents are known to have an elevated rate of substitution, compared to most of the mammals (Li et al., 1996; Weinreich, 2001).”
BackgroundDeterminants of Mutation Rate Variation in the Human Germline
Ségurel, L., Wyman, M. J., & Przeworski, M. (2014) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-031714-125740 · Cited by 289 · see citing works
Determinants of rate variation in mammalian DNA sequence evolution.
Bromham, L., Rambaut, A., & Harvey, P. H. (1996) · Journal of Molecular Evolution · doi:10.1007/bf02202109 · Cited by 291 · see citing works
Белый, В. А., Levine, A. J., & Skalka, A. M. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001030 · Cited by 292 · see citing works
“12% of nucleotides per million years in primates to 2–4 times that value in rodents [13,14,15,16].”
BackgroundThe dynamics of chromosome evolution in birds and mammals
Burt, D. W., Bruley, C., Dunn, I., Jones, C. T., Ramage, A. D., Law, A. S., Morrice, D., Paton, I. R., Smith, J., Windsor, D., et al. (1999) · Nature · doi:10.1038/46555 · Cited by 288 · see citing works
“Our findings on rates of chromosomal rearrangement show similarities to the comparison of nucleotide substitution rate”
ResultCompositional differences within and between eukaryotic genomes
Karlin, S., & Mrázek, J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.19.10227 · Cited by 264 · see citing works
Overlooked roles of DNA damage and maternal age in generating human germline mutations
Gao, Z., Moorjani, P., Sasani, T. A., Pedersen, B. S., Quinlan, A. R., Jorde, L. B., Amster, G., & Przeworski, M. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901259116 · Cited by 229 · see citing works
“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).”
BackgroundLartillot, N., & Poujol, R. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msq244 · Cited by 243 · see citing works
Rochette, C., Gilbert, N., & Simard, L. R. (2001) · Human Genetics · doi:10.1007/s004390100473 · Cited by 241 · see citing works
MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences
Schwartz, S. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg579 · Cited by 233 · see citing works
Geraldes, A., Basset, P., GIBSON, B., Smith, K. L., Harr, B., Yu, H., Bulatova, N., Ziv, Y., & Nachman, M. W. (2008) · Molecular Ecology · doi:10.1111/j.1365-294x.2008.04005.x · Cited by 227 · see citing works
“However, we note that our estimates per year are in good agreement with previous estimates (e.g. Li et al. 1996).”
InfluentialEvolutionary dynamics of coding and non-coding transcriptomes
Necşulea, A., & Kaessmann, H. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3802 · Cited by 222 · see citing works
Molecular Dating and Biogeography of the Early Placental Mammal Radiation
Eizirik, E. (2001) · Journal of Heredity · doi:10.1093/jhered/92.2.212 · Cited by 220 · see citing works
“A potentially confounding aspect of molecular dating methods would be rate heterogeneity among lineages, which has been apparent in some studies of placental mammals including rodents (e.g., Gu and Li 1992; Li et al. 1996).”
ResultLi, W. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00354-4 · Cited by 224 · see citing works
Self-citationTorre, A. R. D. L., Li, Z., de Peer, Y. V., & Ingvarsson, P. K. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx069 · Cited by 219 · see citing works
“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).”
BackgroundBromham, L. D. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0014 · Cited by 211 · see citing works
Taller plants have lower rates of molecular evolution
Lanfear, R., Ho, S. Y. W., Davies, T. J., Moles, A. T., Aarssen, L. W., Swenson, N. G., Warman, L., Zanne, A. E., & Allen, A. P. (2013) · Nature Communications · doi:10.1038/ncomms2836 · Cited by 208 · see citing works
A global survey of haplotype frequencies and linkage disequilibrium at the DRD2 locus
Kidd, K., Morar, B., Castiglione, C., Zhao, H.-Y., Pakstis, A., Speed, W. C., Bonné-Tamir, B., Lu, R., Goldman, D., Lee, C., et al. (1998) · Human Genetics · doi:10.1007/s004390050809 · Cited by 202 · see citing works
“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
Gaut, B. S. (1998) · Springer eBooks · doi:10.1007/978-1-4899-1751-5_4 · Cited by 198 · see citing works
Sensitivity of the relative-rate test to taxonomic sampling
Robinson‐Rechavi, M., Gouy, M., Gautier, C., & Mouchiroud, D. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026016 · Cited by 194 · see citing works
John, U. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg105 · Cited by 194 · see citing works
“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).”
BackgroundShao, R. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg176 · Cited by 195 · see citing works
Nei, M., Kumar, S., & Takahashi, K. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.21.12390 · Cited by 192 · see citing works
Burgess, R., & Yang, Z. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn148 · Cited by 184 · see citing works
“There is considerable evidence for a rate difference between OWMs and the great apes (Goodman 1961; Li et al. 1996; Yi et al. 2002; Kim et al. 2006).”
BackgroundTakahata, N., & Satta, Y. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.9.4811 · Cited by 177 · see citing works
Doris, P. A. (2002) · Hypertension · doi:10.1161/hy0202.104087 · Cited by 179 · see citing works
Sex biases in the mutation rate
Hurst, L. D., & Ellegren, H. (1998) · Trends in Genetics · doi:10.1016/s0168-9525(98)01577-7 · Cited by 171 · see citing works
Improving pregnancy outcomes in humans through studies in sheep
Morrison, J. L., Berry, M. J., Botting, K. J., Darby, J. R. T., Frasch, M. G., Gatford, K. L., Giussani, D. A., Gray, C. L., Harding, R., Herrera, E. A., et al. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00391.2017 · Cited by 171 · see citing works
Higher origination and extinction rates in larger mammals
Liow, L. H., Fortelius, M., Bingham, E., Lintulaakso, K., Mannila, H., Flynn, L., & Stenseth, N. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709763105 · Cited by 166 · see citing works
The Patterns and Causes of Variation in Plant Nucleotide Substitution Rates
Gaut, B. S., Yang, L., Takuno, S., & Eguiarte, L. E. (2011) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-102710-145119 · Cited by 162 · see citing works
“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.”
BackgroundKidd, J. R., PAKSTIS, A. J., Zhao, H., Lu, R., Okonofua, F. E., Odunsi, A., Grigorenko, E. L., Bonné, B., Friedlaender, J. S., Schulz, L. O., et al. (2000) · The American Journal of Human Genetics · doi:10.1086/302952 · Cited by 160 · see citing works
“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).”
BackgroundBusch, J. D., Waser, P. M., & DeWoody, J. A. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03283.x · Cited by 161 · see citing works
“This estimate might be low for rodents, given their accelerated rate of molecular evolution (Martin & Palumbi 1993; Li et al. 1996; Triant & DeWoody 2006).”
BackgroundEvidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees
de Groot, N. G., Otting, Ń., Doxiadis, G. G. M., Balla-Jhagjhoorsingh, S. S., Heeney, J. L., van Rood, J. J., Gagneux, P., & Bontrop, R. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182420799 · Cited by 161 · see citing works
Crandall, E. D., Sbrocco, E. J., DeBoer, T. S., Barber, P. H., & Carpenter, K. E. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr227 · Cited by 157 · see citing works
Molecular evolution meets the genomics revolution
Wolfe, K. H., & Li, W. (2003) · Nature Genetics · doi:10.1038/ng1088 · Cited by 153 · see citing works
“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.”
BackgroundSelf-citationSteiper, M. E., Young, N. M., & Sukarna, T. Y. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407270101 · Cited by 149 · see citing works
Interpreting the Dependence of Mutation Rates on Age and Time
Gao, Z., Wyman, M. J., Sella, G., & Przeworski, M. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002355 · Cited by 145 · see citing works
“Therefore, the general observation that substitution rate in mammals tends to decrease with increasing generation times [7,10,16] is not necessarily expected; in fact, its existence requires very specific conditions on ontogenesis to hold (shown in Fig 3B).”
BackgroundInfluentialModel Averaging and Bayes Factor Calculation of Relaxed Molecular Clocks in Bayesian Phylogenetics
Li, W. L. S., & Drummond, A. J. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr232 · Cited by 145 · see citing works
“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).”
BackgroundSelf-citationRowe, D. L., & Honeycutt, R. L. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004080 · Cited by 146 · see citing works
“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).”
BackgroundResultTime scale of eutherian evolution estimated without assuming a constant rate of molecular evolution.
Hasegawa, M., Thorne, J. L., & Kishino, H. (2003) · Genes & Genetic Systems · doi:10.1266/ggs.78.267 · Cited by 145 · see citing works
Kai, W., Kikuchi, K., Tohari, S., Chew, A. K., Tay, A., Fujiwara, A., Hosoya, S., Suetake, H., Naruse, K., Brenner, S., et al. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr041 · Cited by 146 · see citing works
Evidence for a selectively favourable reduction in the mutation rate of the X chromosome
McVean, G. T., & Hurst, L. D. (1997) · Nature · doi:10.1038/386388a0 · Cited by 146 · see citing works
High and Variable Rates of Repeat-Mediated Mitochondrial Genome Rearrangement in a Genus of Plants
Cole, L. W., Guo, W., Mower, J. P., & Palmer, J. D. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy176 · Cited by 144 · see citing works
Vagaries of the molecular clock.
Ayala, F. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.15.7776 · Cited by 140 · see citing works
Ogino, S., Wilson, R. B., & Gold, B. (2004) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201288 · Cited by 143 · see citing works
Recent origin of HLA-DRB1 alleles and implications for human evolution
Bergström, T. F., Josefsson, A., Erlich, H. A., & Gyllensten, U. B. (1998) · Nature Genetics · doi:10.1038/ng0398-237 · Cited by 142 · see citing works
Low Levels of Nucleotide Diversity in Mammalian Y Chromosomes
Hellborg, L. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msh008 · Cited by 141 · see citing works
“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).”
BackgroundInfluentialEvolutionary Genetics and Genetic Variation of Haplodiploids and X-Linked Genes
Hedrick, P. W., & Parker, J. D. (1997) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.28.1.55 · Cited by 139 · see citing works
Slow Molecular Clocks in Old World Monkeys, Apes, and Humans
Yi, S. V., Ellsworth, D. L., & Li, W. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004043 · Cited by 137 · see citing works
“The average ratio of the substitution rate in the OWM lineage to that in the Homo lineage is 1.33, which ratios of germ cell division in mice and primates roughly correspond to the estimated male-to-female ratios of the mutation rate (Li et al. 1996).”
BackgroundMethodInfluentialSelf-citationLife history effects on the molecular clock of autosomes and sex chromosomes
Amster, G., & Sella, G. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515798113 · Cited by 134 · see citing works
“Proc Natl Acad Sci USA 109(39):15716–15721.”
BackgroundInfluentialБелый, В. А., Levine, A. J., & Skalka, A. M. (2010) · Journal of Virology · doi:10.1128/jvi.01789-10 · Cited by 136 · see citing works
“14% per million years of evolution (8), we arrive at 90 million years as the theoretical limit for the oldest sequences that can be identified using our methods.”
BackgroundPawlowski, J. W., Bolívar, I., Fahrni, J. F., de Vargas, C., Gouy, M., & Zaninetti, L. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025786 · Cited by 133 · see citing works
Site specific rates of mitochondrial genomes and the phylogeny of eutheria.
Kjer, K. M., & Honeycutt, R. L. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-8 · Cited by 132 · see citing works
“terms of morphological diversification [4] and molecular divergence [5-7] is a trademark of the various orders and families of mammals, especially within the Eutheria, and this has complicated efforts to resolve phylogenetic relationships among the higher categories of mammals.”
BackgroundCytochrome b Phylogeny and the Taxonomy of Great Apes and Mammals
Castresana, J. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003825 · Cited by 130 · see citing works
“Some authors have postulated that the metabolic rate (Martin and Palumbi 1993; Nunn and Stanley 1998) or the generation time (Bromham, Rambaut, and Harvey 1996; Li et al. 1996), which, in turn, are correlated with the body mass, could be responsible for the different rates.”
BackgroundMitochondrial DNA Rates and Biogeography in European Newts (Genus Euproctus)
Caccone, A., Milinkovitch, M. C., Sbordoni, V., & Powell, J. R. (1997) · Systematic Biology · doi:10.1093/sysbio/46.1.126 · Cited by 126 · see citing works
“Although several hypotheses, such as generation time (Wu and Li, 1985; Li et al., 1996), DNA repair efficiency (Britten, 1986), nucleotide generation time (Martin et al.”
BackgroundGrowing up with dinosaurs: molecular dates and the mammalian radiation
Bromham, L., Phillips, M. J., & Penny, D. (1999) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(98)01507-9 · Cited by 127 · see citing works
Genome analyses substantiate male mutation bias in many species
Sayres, M. A. W., & Makova, K. D. (2011) · BioEssays · doi:10.1002/bies.201100091 · Cited by 124 · see citing works
“free radicals present in cells) in generating mutations is significant [7, 8].”
BackgroundRooney, A. P., & Zhang, J. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026153 · Cited by 124 · see citing works
Heterogeneous Models Place the Root of the Placental Mammal Phylogeny
Morgan, C. C., Foster, P. G., Webb, A. E., Pisani, D., McInerney, J. O., & O’Connell, M. J. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst117 · Cited by 123 · see citing works
“Smaller, shorter-lived mammals with high metabolic rates and short germ-line generation times accumulate mutations at a higher rate (Li et al. 1996).”
Muse, S. V., & Gaut, B. S. (1997) · Genetics · doi:10.1093/genetics/146.1.393 · Cited by 118 · see citing works
Thybert, D., Roller, M., Navarro, F. C. P., Fiddes, I., Streeter, I., Feig, C., Martín‐Gálvez, D., Kolmogorov, M., Janoušek, V., Akanni, W. A., et al. (2018) · Genome Research · doi:10.1101/gr.234096.117 · Cited by 111 · see citing works
“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.”
Thomas, J. A., Welch, J. J., Woolfit, M., & Bromham, L. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510251103 · Cited by 117 · see citing works
Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements
Nikolaev, S. I., Montoya‐Burgos, J. I., Popadin, K. Y., Parand, L., Margulies, E. H., & Antonarakis, S. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705658104 · Cited by 115 · see citing works
Kehrer‐Sawatzki, H., & Cooper, D. N. (2006) · Human Mutation · doi:10.1002/humu.20420 · Cited by 112 · see citing works
“According to the ‘‘generation-time effect hypothesis’’ [Goodman, 1962; Li et al., 1996], most germline mutations originate from errors in DNA replication.”
BackgroundComparative analysis of phylogenetic and fishing effects in life history patterns of teleost fishes
Rochet, M.-J., Cornillon, P., Sabatier, R., & Pontier, D. (2000) · Oikos · doi:10.1034/j.1600-0706.2000.910206.x · Cited by 107 · see citing works
“For a given trait, evolutionary rates vary between branches of a phylogenetic tree (Aota and Ikemura 1986, Britten 1986, Catzeflis et al. 1987, Li et al. 1996, Mindell and Thacker 1996), and they also vary with time along a given branch (Svensson 1997).”
BackgroundEnard, W., & Pääbo, S. (2004) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.5.061903.180040 · Cited by 108 · see citing works
“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).”
BackgroundEvidence for a Slowed Rate of Molecular Evolution in the Order Acipenseriformes
Krieger, J., & Fuerst, P. A. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004146 · Cited by 106 · see citing works
Variable molecular clocks in hominoids
Elango, N., Thomas, J. W., Program§, N. C. S., & Yi, S. V. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510716103 · Cited by 105 · see citing works
Huchon, D., Catzeflis, F. M., & Douzery, E. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026140 · Cited by 102 · see citing works
Nygren, 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 · see citing works
LIFE HISTORY AND THE MALE MUTATION BIAS
Bartosch-Härlid, A., Berlin, S., Smith, N. G. C., Møller, A. P., & Ellegren, H. (2003) · Evolution · doi:10.1554/03-036 · Cited by 99 · see citing works
“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 · see citing works
Lercher, M. J., Williams, E. J. B., & Hurst, L. D. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003744 · Cited by 97 · see citing works
“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 · see citing works
“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 · see citing works
Heterogeneous Genomic Molecular Clocks in Primates
Kim, S., Elango, N., Warden, C., Vigoda, E., & Yi, S. V. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020163 · Cited by 92 · see citing works
“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 93 · see citing works
“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 93 · see citing works
“…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 · see citing works
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 91 · see citing works
Insights from human/mouse genome comparisons
Pennacchio, L. A. (2003) · Mammalian Genome · doi:10.1007/s00335-002-4001-1 · Cited by 86 · see citing works
“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 · see citing works
“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 · see citing works
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 81 · see citing works
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 · see citing works
- 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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