Skip to main content
Log in

The Concept of the Modern Molecular Clock and Experience in Estimating Divergence Times of Eulipotyphla and Rodentia

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

Almost 60 years have passed since the degree of DNA difference between two species was discovered to be a function of the time since their divergence. Later, it became clear that there is no universal molecular clock and the rate of molecular evolution varies greatly depending on the gene and phylogenetic lineage, correlating with biological characteristics (generation length, body size, and fertility) and features of the genome. The development of the molecular clock concept is associated with progress in methods that allow the degree of inconstancy of the rate of molecular evolution to be taken into account and measured. Currently, dating is mostly performed using Relaxed Clock methods, which rely on various models of the evolution rate (for example, with or without autocorrelation of rates in adjacent branches). Another relevant factor that allows reduction of the errors of molecular dating is the increase in the amount of data up to the genomic level, which enhances the requirements for computationally efficient algorithms and the methods of data partitioning. A separate problem is the time dependence of evolutionary rate estimates (the phenomenon of rate decay), which is especially important for the analysis of recent history. In the absence of an adequate sequence evolution model, time estimates can be significantly biased, which often affects the results obtained with mtDNA. One of the most important trends is the development of methods for obtaining calibration information: the more complete use of the constantly and rapidly growing volume of paleontological data, the analysis of paleoDNA, and other variants of heterochronous data. Despite the fact that the accuracy of estimates of the levels of molecular divergences continues to grow, the uncertainty in dating persists, largely due to the ambiguity of calibrations and the shortcomings of existing models of DNA sequence evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Aiewsakun, P. and Katzourakis, A., Time-dependent rate phenomenon in viruses, J. Virol., 2016, vol. 90, no. 16, pp. 7184–7195.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Allio, R., Donega, S., Galtier, N., and Nabholz, B., Large variation in the ratio of mitochondrial to nuclear mutation rate across animals: implications for genetic diversity and the use of mitochondrial DNA as a molecular marker, Mol. Biol. Evol., 2017, vol. 34, no. 11, pp. 2762–2772.

    Article  CAS  PubMed  Google Scholar 

  3. Álvarez-Carretero, S. and Dos Reis, M., Bayesian phylogenomic dating, in The Molecular Evolutionary Clock, Cham: Springer, 2020, pp. 221–249.

    Google Scholar 

  4. Angelis, K., Álvarez-Carretero, S., dos Reis, M., and Yang, Z., An evaluation of different partitioning strategies for Bayesian estimation of species divergence times, Syst. Biol., 2018, vol. 67, no. 1, pp. 61–77.

    Article  CAS  PubMed  Google Scholar 

  5. Arbogast, B.S., Edwards, S.V., Wakeley, J., Beerli, P., and Slowinski, J.B., Estimating divergence times from molecular data on phylogenetic and population genetic timescales, Annu. Rev. Ecol. Syst., 2002, vol. 33, no. 1, pp. 707–740.

    Article  Google Scholar 

  6. Archibald, J.D. and Deutschman, D.H., Quantitative analysis of the timing of the origin and diversification of extant placental orders, J. Mamm. Evol., 2001, vol. 8, no. 2, pp. 107–124.

    Article  Google Scholar 

  7. Archibald, J.D., Averianov, A.O., and Ekdale, E.G., Late cretaceous relatives of rabbits, rodents, and other extant eutherian mammals, Nature, 2001, vol. 414, no. 6859, pp. 62–65.

    Article  CAS  PubMed  Google Scholar 

  8. Aris-Brosou, S. and Yang, Z., Effects of models of rate evolution on estimation of divergence dates with special reference to the metazoan 18S ribosomal RNA phylogeny, Syst. Biol., 2002, vol. 51, no. 5, pp. 703–714.

    Article  PubMed  Google Scholar 

  9. Bannikova, A.A., Molecular evolution and problems of phylogenetic reconstruction of true insectivores (Mammalia: Eulipotyphla), Doctoral (Biol.) Dissertation, Moscow: Moscow State University, 2019.

  10. Bannikova, A.A., Lebedev, V.S., Lissovsky, A.A., Matrosova, V., Abramson, N.I., et al., Molecular phylogeny and evolution of the Asian lineage of vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial cytb sequence, Biol. J. Linn. Soc., 2010a, vol. 99, no. 3, pp. 595–613.

    Article  Google Scholar 

  11. Bannikova, A.A., Dokuchaev, E.N., Yudina, E.V., Bobretzov, A.V., Sheftel, B.I., and Lebedev, V.S., Holarctic phylogeography of the tundra shrew (Sorex tundrensis) based on mitochondrial genes, Biol. J. Linn. Soc., 2010b, vol. 101, no. 3, pp. 721–746.

    Article  Google Scholar 

  12. Bannikova, A.A., Lebedev, V.S., Abramov, A.V., and Rozhnov, V.V., Contrasting evolutionary history of hedgehogs and gymnures (Mammalia: Erinaceomorpha) as inferred from a multigene study, Biol. J. Linn. Soc., 2014, vol. 112, pp. 499–519.

    Article  Google Scholar 

  13. Bannikova, A.A., Zemlemerova, E.D., Colangelo, P., Sözen, M., Sevindik, M., et al., An underground burst of diversity - a new look at the phylogeny and taxonomy of the genus Talpa Linnaeus, 1758 (Mammalia: Talpidae) as revealed by nuclear and mitochondrial genes, Zool. J. Linn. Soc., 2015, vol. 175, no. 4, pp. 930–948.

    Article  Google Scholar 

  14. Bannikova, A.A., Chernetskaya, D., Raspopova, A., Alexandrov, D., Fang, Y., et al., Evolutionary history of the genus Sorex (Soricidae, Eulipotyphla) as inferred from multigene data, Zool. Scr., 2018, vol. 47, no. 5, pp. 518–538.

    Article  Google Scholar 

  15. Bannikova, A.A., Zemlemerova, E.D., Lebedev, V.S., and Lavrenchenko, L.A., The phylogenetic relationships within the Eastern Afromontane clade of Crocidura based on mitochondrial and nuclear data, Mamm. Biol., 2021, vol. 101, рр. 1005–1018. https://doi.org/10.1007/s42991-021-00120-7

  16. Barrera-Redondo, J., Ramírez-Barahona, S., and Eguiarte, L.E., Rates of molecular evolution in tree ferns are associated with body size, environmental temperature, and biological productivity, Evolution, 2018, vol. 72, no. 5, pp. 1050–1062.

    Article  PubMed  Google Scholar 

  17. Benton, M.J. and Ayala, F.J., Dating the tree of life, Science, 2003, vol. 300, no. 5626, pp. 1698–1700.

    Article  CAS  PubMed  Google Scholar 

  18. Benton, M.J. and Donoghue, P.C.J., Paleontological evidence to date the tree of life, Mol. Biol. Evol., 2007, vol. 24, no. 1, pp. 26–53.

    Article  CAS  PubMed  Google Scholar 

  19. Benton, M.J., Donoghue, P.C.J., and Asher, R.J., Calibrating and constraining molecular clocks, in The Timetree of Life, New-York: Oxford Univ. Press, 2009, pp. 35–86.

  20. Bertorelle, G., Benazzo, A., and Mona, S., ABC as a flexible framework to estimate demography over space and time: some cons, many pros, Mol. Ecol., 2010, vol. 19, no. 13, pp. 2609–2625.

    Article  CAS  PubMed  Google Scholar 

  21. Bininda-Emonds, O.R.P., Cardillo, M., Jones, K.E., MacPhee R.D.E., Beck R.M.D., et al., The delayed rise of present-day mammals, Nature, 2007, vol. 446, no. 7135, pp. 507–512.

    Article  CAS  PubMed  Google Scholar 

  22. Bird, A.P., DNA methylation and the frequency of CpG in animal DNA, Nucleic Acid Res., 1980, vol. 8, no. 7, pp. 1499–1504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Brandley, M.C., Wang, Y., Guo, X., De Oca, A.N.M., Fería-Ortíz, M., et al., Accommodating heterogenous rates of evolution in molecular divergence dating methods: An example using intercontinental dispersal of Plestiodon (Eumeces) lizards, Syst. Biol., 2011, vol. 60, no. 1, pp. 3–15.

    Article  CAS  PubMed  Google Scholar 

  24. Bromham, L., Molecular clocks in reptiles: life history influences rate of molecular evolution, Mol. Biol. Evol., 2002, vol. 19, no. 3, pp. 302–309.

    Article  CAS  PubMed  Google Scholar 

  25. Bromham, L., The genome as a life-history character: Why rate of molecular evolution varies between mammal species, Philos. Trans. Roy. Soc. B. Biol. Sci., 2011, vol. 366, no. 1577, pp. 2503–2513.

    Article  Google Scholar 

  26. Bromham, L., Causes of variation in the rate of molecular evolution, in The Molecular Evolutionary Clock, Cham: Springer, 2020, pp. 45–64.

    Google Scholar 

  27. Bromham, L. and Penny, D., The modern molecular clock, Nat. Rev. Genet., 2003, vol. 4, no. 3, pp. 216–224.

    Article  CAS  PubMed  Google Scholar 

  28. Bromham, L., Rambaut, A., and Harvey, P.H., Determinants of rate variation in mammalian DNA sequence evolution, J. Mol. Evol., 1996, vol. 43, no. 6, pp. 610–621.

    Article  CAS  PubMed  Google Scholar 

  29. Bromham, L., Rambaut, A., Fortey, R., Cooper, A., and Penny, D., Testing the Cambrian explosion hypothesis by using a molecular dating technique, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, no. 21, pp. 12386–12389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bromham, L., Penny, D., Rambaut, A., and Hendy, M.D., The power of relative rates tests depends on the data, J. Mol. Evol., 2000, vol. 50, no. 3, pp. 296–301.

    Article  CAS  PubMed  Google Scholar 

  31. Bromham, L., Hua, X., Lanfear, R., and Cowman, P.F., Exploring the relationships between mutation rates, life history, genome size, environment, and species richness in flowering plant, The American Naturalist, 2015, vol. 185, no. 4, pp. 507–524.

    Article  PubMed  Google Scholar 

  32. Bromham, L., Duchêne, S., Hua, X., Ritchie, A.M., Duchêne, D.A., and Ho, S.Y.W., Bayesian molecular dating: opening up the black box, Biol. Rev., 2018, vol. 93, no. 2, pp. 1165–1191.

    Article  PubMed  Google Scholar 

  33. Brown, R.P. and Yang, Z., Rate variation and estimation of divergence times using strict and relaxed clocks, BMC Evol. Biol., 2011, vol. 11. https://doi.org/10.1186/1471-2148-11-271

  34. Brown, W.M., George, M., Jr., and Wilson, A.C., Rapid evolution of animal mitochondrial DNA, Proc. Natl. Acad. Sci. USA, 1979, vol. 76, no. 4, pp. 1967–1971.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Butler, P.M., On the evolution of the skull and teeth in the Erinaceidae, with special reference to fossil material in the British, Proc. Zool. Soc. London, 1948, vol. 118, no. 2, pp. 446–500.

    Article  Google Scholar 

  36. Chintalapati, M. and Moorjani, P., Evolution of the mutation rate across primates, Curr. Opin. Genet. Dev., 2020, vol. 62, pp. 58–64.

    Article  CAS  PubMed  Google Scholar 

  37. Cosson, J.-F., Hutterer, R., Libois, R., Sara, M., Taberlet, P., and Vogel, P., Phylogeographical footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew, Crocidura russula (Mammalia: Soricidae), Mol. Ecol., 2005, vol. 14, no. 4, pp. 1151–1162.

    Article  CAS  PubMed  Google Scholar 

  38. Cracraft, J., Houde, P., Ho, S.Y.W., Mindell, D.P., Fjeldså, J., et al., Response to comment on “Whole-genome analyses resolve early branches in the tree of life of modern birds,”” Science, 2015, vol. 349, no. 6255. https://doi.org/10.1126/science.aab1578

  39. De Baets, K., Antonelli, A., and Donoghue, P.C.J., Tectonic blocks and molecular clocks, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2016, vol. 371, no. 1699. https://doi.org/10.1098/rstb.2016.0098

  40. Debruyne, R. and Poinar, H.N., Time dependency of molecular rates in ancient DNA data sets, a sampling artifact?, Syst. Biol., 2009, vol. 58, no. 3, pp. 348–360.

    Article  CAS  PubMed  Google Scholar 

  41. Depéret, C., Recherches sur la succession des Faunes de Vertébrés miocénes de la vallée du Rhone, Arch. Mus. Hist. Nat. Lyon, 1887, vol. 4, pp. 45–313.

    Google Scholar 

  42. Donoghue, P.C. and Benton, M.J., Rocks and clocks: calibrating the tree of life using fossils and molecules, Trends Ecol. Evol., 2007, vol. 22, no. 8, pp. 424–431.

    Article  PubMed  Google Scholar 

  43. Doolittle, R.F. and Blombäck, B., Amino-acid sequence investigations of fibrinopeptides from various mammals: evolutionary implications, Nature, 1964, vol. 202, no. 4928, pp. 147–152.

    Article  CAS  PubMed  Google Scholar 

  44. Dornburg, A., Townsend, J.P., Friedman, M., and Near, T.J., Phylogenetic informativeness reconciles ray-finned fish molecular divergence times, BMC Evol. Biol., 2014, vol. 14, no. 1. https://doi.org/10.1186/s12862-014-0169-0

  45. Dos Reis, M. and Yang, Z., The unbearable uncertainty of Bayesian divergence time estimation, Journal of Systematics and Evolution, 2013, vol. 51, no. 1, pp. 30–43.

    Article  Google Scholar 

  46. Dos Reis, M., Inoue, J., Hasegawa, M., Asher, R.J., Donoghue, P.C., and Yang, Z., Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny, Proc. R. Soc. B, 2012, vol. 279, no. 1742, pp. 3491–3500.

  47. Dos Reis, M., Zhu, T., and Yang, Z., The impact of the rate prior on Bayesian estimation of divergence times with multiple loci, Syst. Biol., 2014, vol. 63, no. 4, pp. 555–565.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Dos Reis, M., Thawornwattana, Y., Angelis, K., Telford, M.J., Donoghue, P.C.J., and Yang, Z., Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales, Curr. Biol., 2015, vol. 25, no. 22, pp. 2939–2950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Dos Reis, M., Donoghue, P.C.J., and Yang, Z., Bayesian molecular clock dating of species divergences in the genomics era, Nat. Rev. Genet., 2016, vol. 17, no. 2, pp. 71–80.

    Article  CAS  PubMed  Google Scholar 

  50. Dos Reis, M.D., Gunnell, G.F., Barba-Montoya, J., Wilkins, A., Yang, Z., and Yoder, A.D., Using phylogenomic data to explore the effects of relaxed clocks and calibration strategies on divergence time estimation: primates as a test case, Syst. Biol., 2018, vol. 67, no. 4, pp. 594–615.

    Article  Google Scholar 

  51. Douady, C. and Douzery, E., Molecular estimation of eulipotyphlan divergence times and the evolution of “Insectivora,” Mol. Phylogenet. Evol., 2003, vol. 28, no. 2, pp. 285–296.

    Article  CAS  PubMed  Google Scholar 

  52. Douady, C.J., Chatelier, P.I., Madsen, O., De Jong, W.W., Catzeflis, F., et al., Molecular phylogenetic evidence confirming the Eulipotyphla concept and in support of hedgehogs as the sister group to shrews, Mol. Phylogenet. Evol., 2002, vol. 25, no. 1, pp. 200–209.

    Article  CAS  PubMed  Google Scholar 

  53. Drake, J.W., Charlesworth, B., Charlesworth, D., and Crow, J.F., Rates of spontaneous mutation, Genetics, 1998, vol. 148, no. 4, pp. 1667–1686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Drummond, A.J. and Suchard, M.A., Bayesian random local clocks, or one rate to rule them all, BMC Biol., 2010, vol. 8. https://doi.org/10.1186/1741-7007-8-114

  55. Drummond, A.J., Ho, S.Y.W., Phillips, M.J., and Rambaut, A., Relaxed phylogenetics and dating with confidence, PLOS Biol., 2006, vol. 4, no. 5. https://doi.org/10.1371/journal.pbio.0040088

  56. Drummond, A.J., Suchard, M.A., Xie, D., and Rambaut, A., Bayesian phylogenetics with BEAUti and the BEAST 1.7, Mol. Biol. Evol., 2012, vol. 29, no. 8, pp. 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Duchêne, D. and Bromham, L., Rates of molecular evolution and diversification in plants: chloroplast substitution rates correlate with species richness in the proteaceae, BMC Evol. Biol., 2013, vol. 13. https://doi.org/10.1186/1471-2148-13-65

  58. Duchêne, S., Lanfear, R., and Ho, S.Y.W., The impact of calibration and clock-model choice on molecular estimates of divergence times, Mol. Phylogenet. Evol., 2014, vol. 78, pp. 277–289.

    Article  PubMed  Google Scholar 

  59. Duchêne, S., Holt, K.E., Weill, F.-X., Le Hello, S., Hawkey, J., et al., Genome-scale rates of evolutionary change in bacteria, Microb. Genomics, 2016, vol. 2, no. 11. https://doi.org/10.1099/mgen.0.000094

  60. Duffy, S., Shackelton, L.A., and Holmes, E.C., Rates of evolutionary change in viruses: patterns and determinants, Nat. Rev. Genet., 2008, vol. 9, no. 4, pp. 267–276.

    Article  CAS  PubMed  Google Scholar 

  61. Duret, L. and Arndt, P.F., The impact of recombination on nucleotide substitutions in the human genome, PLoS Genet., 2008, vol. 4, no. 5. https://doi.org/10.1371/journal.pgen.1000071

  62. Easteal, S. and Herbert, G., Molecular evidence from the nuclear genome for the time frame of human evolution, J. Mol. Evol., 1997, vol. 44, suppl. 1, pp. S121–S132.

    Article  CAS  PubMed  Google Scholar 

  63. Easteal, S., Collet, C., Betty, D., and Ashley, M.V., Mammalian Molecular Clock, Austin: R.G. Landes Co, 1995.

    Google Scholar 

  64. Eldredge, N. and Gould, S.J., Punctuated equilibria: an alternative to phyletic gradualism, in Models in Paleobiology, San Francisco: Freeman, 1972, pp. 82–115.

    Google Scholar 

  65. Emerson, B.C., Alarm bells for the molecular clock? No support for Ho et al.’s model of time-dependent molecular rate estimates, Syst. Biol., 2007, vol. 56, no. 2, pp. 337–345.

    Article  CAS  PubMed  Google Scholar 

  66. Emerson, B.C. and Hickerson, M.J., Lack of support for the time-dependent molecular evolution hypothesis, Mol. Ecol., 2015, vol. 24, no. 4, pp. 702–709.

    Article  PubMed  Google Scholar 

  67. Felsenstein, J., Evolutionary trees from DNA sequences: a maximum likelihood approach, J. Mol. Evol., 1981, vol. 17, no. 6, pp. 368–376.

    Article  CAS  PubMed  Google Scholar 

  68. Felsenstein, J., Inferring Phylogenies, Sunderland: Sinauer Associates, 2004.

    Google Scholar 

  69. Fisher, R.A., The measurement of selective intensity, Proc. R. Soc. B, 1936, vol. 121, pp. 58–62.

    Google Scholar 

  70. Fitch, W.M. and Beintema, J.J., Correcting parsimonious trees for unseen nucleotide substitutions: the effect of dense branching as exemplified by ribonuclease, Mol. Biol. Evol., 1990, vol. 7, no. 5, pp. 438–443.

    CAS  PubMed  Google Scholar 

  71. Fleischer, R.C., McIntosh, C.E., and 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., 1998, vol. 7, no. 4, pp. 533–545.

    Article  CAS  PubMed  Google Scholar 

  72. Foster, C.S.P., Sauquet, H., Van Der Merwe, M., McPherson, H., Rossetto, M., and Ho, S.Y.W., Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale, Syst. Biol., 2016, vol. 66, no. 3, pp. 338–351.

    Google Scholar 

  73. Frost, D.R., Wozencraft, W.C., and Hoffmann, R.S., Phylogenetic Relationships of Hedgehogs and Gymnures (Mammalia: Insectivora: Erinaceidae), Washington: Smithsonian Institution Press, 1991.

    Book  Google Scholar 

  74. Fu, Y., Foden, J.A., Khayter, C., Maeder, M.L., Reyon, D., et al., High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells, Nat. Biotechnol., 2013, vol. 31, no. 9, pp. 822–826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Galtier, N., Enard, D., Radondy, Y., Bazin, E., and Bel-khir, K., Mutation hot spots in mammalian mitochondrial DNA, Genome Res., 2006, vol. 16, no. 2, pp. 215–222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Galtier, N., Jobson, R.W., Nabholz, B., Glemin, S., and Blier, P.U., Mitochondrial whims: metabolic rate, longevity and the rate of molecular evolution, Biol. Lett., 2009, vol. 5, no. 3, pp. 413–416.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Gandolfo, M., Nixon, K.C., and Crepet, W.L., Selection of fossils for calibration of molecular dating models, Ann. Mo. Bot. Gard., 2008, vol. 95, no. 1, pp. 34–42.

    Article  Google Scholar 

  78. Gao, Z., Wyman, M.J., Sella, G., and Przeworski, M., Interpreting the dependence of mutation rates on age and time, PLoS Biol., 2016, vol. 14, no. 1. https://doi.org/10.1371/journal.pbio.1002355

  79. Gavryushkina, A. and Zhu, C., Total-evidence dating and the fossilized birth-death model, in The Molecular Evolutionary Clock, Cham: Springer, 2020, pp. 175–197.

    Google Scholar 

  80. Gavryushkina, A., Welch, D., Stadler, T., and Drummond, A.J., Bayesian inference of sampled ancestor trees for epidemiology and fossil calibration, PLoS Comput. Biol., 2014, vol. 10, no. 12. https://doi.org/10.1371/journal.pcbi.1003919

  81. Gillespie, J.H., The Causes of Molecular Evolution, Oxford: Oxford Univ. Press, 1991.

    Google Scholar 

  82. Gillooly, J.F., Allen, A.P., West, G.B., and Brown, J.H., The rate of DNA evolution: effects of body size and temperature on the molecular clock, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, no. 1, pp. 140–145.

    Article  CAS  PubMed  Google Scholar 

  83. Goodman, M., The role of immunologic differences in the phyletic development of human behavior, Hum. Biol., 1961, vol. 33, no. 2, pp. 131–162.

    CAS  PubMed  Google Scholar 

  84. Goodman, M., Evolution of the immunologic species specificity of human serum proteins, Hum. Biol., 1962, vol. 34, pp. 104–150.

    CAS  PubMed  Google Scholar 

  85. Gould G.C., Hedgehog Phylogeny (Mammalia, Erinaceidae)—The Reciprocal Illumination of the Quick and the Dead, vol. 3131 of American Museum Novitates, New York: Americian Museum of Natural History, 1995.

  86. Guilderson, T.P., Reimer, P.J., and Brown, T.A., The boon and bane of radiocarbon dating, Science, 2005, vol. 307, no. 5708, pp. 362–364.

    Article  CAS  PubMed  Google Scholar 

  87. Guindon, S., Rates and rocks: strengths and weaknesses of molecular dating methods, Front. Genet., 2020, vol. 11. https://doi.org/10.3389/fgene.2020.00526

  88. Haines, W.P., Schmitz, P., and Rubinoff, D., Ancient diversification of Hyposmocoma moths in Hawaii, Nat. Commun., 2014, vol. 5. https://doi.org/10.1038/ncomms4502

  89. Haldane, J.B.S., The mutation rate of the gene for hemophilia, and its segregation ratios in males and females, Ann. Eugenics, 1947, vol. 13, no. 4, pp. 262–271.

    Article  CAS  Google Scholar 

  90. Hardouin, E.A. and Tautz, D., Increased mitochondrial mutation frequency after an island colonization: positive selection or accumulation of slightly deleterious mutations?, Biol Lett., 2013, vol. 9, no. 2. https://doi.org/10.1098/rsbl.2012.1123

  91. Hasegawa, M., Kishino, H., and Yano, T., Estimation of branching dates among primates by molecular clocks of nuclear DNA which slowed down in Hominoidea, J. Hum. Evol., 1989, vol. 18, no. 5, pp. 461–476.

    Article  Google Scholar 

  92. Hasegawa, M., Thorne, J.L., and Kishino, H., Time scale of eutherian evolution estimated without assuming a constant rate of molecular evolution, Genes Genet. Syst., 2003, vol. 78, no. 4, pp. 267–283.

    Article  CAS  PubMed  Google Scholar 

  93. Heath, T.A. and Moore, B.R., Bayesian inference of species divergence times, in Bayesian Phylogenetics: Methods, Algorithms and Applications, Boca Raton: CRC Press, 2014, pp. 277–318.

    Google Scholar 

  94. Heath, T.A., Holder, M.T., and Huelsenbeck, J.P., A Dirichlet process prior for estimating lineage-specific substitution rates, Mol. Biol. Evol., 2012, vol. 29, no. 3, pp. 939–955.

    Article  CAS  PubMed  Google Scholar 

  95. Heath, T.A., Huelsenbeck, J.P., and Stadler, T., The fossilized birth-death process for coherent calibration of divergence-time estimates, Proc. Natl. Acad. Sci. USA, 2014, vol. 111, no. 29, pp. E2957–E2966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Hedges, S.B. and Kumar, S., Genomic clocks and evolutionary timescales, Trends Genet., 2003, vol. 19, no. 4, pp. 200–206.

    Article  Google Scholar 

  97. Heled, J. and Drummond, A.J., Bayesian inference of species trees from multilocus data, Mol. Biol. Evol., 2010, vol. 27, no. 3, pp. 570–580.

    Article  CAS  PubMed  Google Scholar 

  98. Henn, B.M., Gignoux, C.R., Feldman, M.W., Joanna, L., and Mountain, J.L., Characterizing the time dependency of human mitochondrial dna mutation rate estimates, Mol. Biol. Evol., 2008, vol. 26, no. 1, pp. 217–230.

    Article  PubMed  Google Scholar 

  99. Hennig, W., Phylogenetic Systematics, Urbana: Univ. Illinois Press, 1966.

    Google Scholar 

  100. Herman, J.S., McDevitt, A.D., Kawałko, A., Jaarola, M., Wójcik, J.M., and Searle, J.B., Land-bridge calibration of molecular clocks and the post-glacial colonization of Scandinavia by the Eurasian field vole Microtus agrestis, PLoS One, 2014, vol. 9, no. 8. https://doi.org/10.1371/journal.pone.0103949

  101. Hipsley, C.A. and Müller, J., Beyond fossil calibrations: Realities of molecular clock practices in evolutionary biology, Front. Genet., 2014, vol. 5. https://doi.org/10.3389/fgene.2014.00138

  102. Ho, S.Y.W., An examination of phylogenetic models of substitution rate variation among lineages, Biol. Lett., 2009, vol. 5, no. 3, p. 421–424.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Ho, S.Y.W., The changing face of the molecular evolutionary clock, Trends Ecol. Evol., 2014, vol. 29, no. 9, pp. 496–503.

    Article  PubMed  Google Scholar 

  104. Ho, S.Y.W., The molecular clock and evolutionary rates across the tree of life, in The Molecular Evolutionary Clock, Cham: Springer, 2020, pp. 3–24.

    Book  Google Scholar 

  105. Ho, S.Y.W. and Phillips, M.J., Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times, Syst. Biol., 2009, vol. 58, no. 3, pp. 367–380.

    Article  PubMed  Google Scholar 

  106. Ho, S.Y.W. and Duchêne, S., Molecular-clock methods for estimating evolutionary rates and timescales, Mol. Ecol., 2014, vol. 23, no. 24, pp. 5947–5965.

    Article  PubMed  Google Scholar 

  107. Ho, S.Y.W., Phillips, M.J., Cooper, A., and Drummond, A.J., Time dependency of molecular rate estimates and systematic overestimation of recent divergence times, Mol. Biol. Evol., 2005, vol. 22, no. 7, pp. 1561–1568.

    Article  CAS  PubMed  Google Scholar 

  108. Ho, S.Y.W., Shapiro, B., Phillips, M.J., Cooper, A., and Drummond, A.J., Evidence for time dependency of molecular rate estimates, Syst. Biol., 2007, vol. 56, no. 3, pp. 515–522.

    Article  PubMed  Google Scholar 

  109. Ho, S.Y.W., Lanfear, R., Bromham, L., Phillips, M.J., Soubrier, J., et al., Time-dependent rates of molecular evolution, Mol. Ecol., 2011, vol. 20, no. 15, pp. 3087–3101.

    Article  PubMed  Google Scholar 

  110. Ho, S.Y.W., Duchêne, S., and Duchêne, D., Simulating and detecting autocorrelation of molecular evolutionary rates among lineages, Mol. Ecol., 2015a, vol. 15, no. 4, pp. 688–696.

    Article  CAS  Google Scholar 

  111. Ho, S.Y.W., Tong, K.J., Foster, C.S.P., Ritchie, A.M., Lo, N., and Crisp, M.D., Biogeographic calibrations for the molecular clock, Biol. Lett., 2015b, vol. 11, no. 8. https://doi.org/10.1098/rsbl.2015.0194

  112. Hodgkinson, A. and Eyre-Walker, A., Variation in the mutation rate across mammalian genomes, Nat. Rev. Genet., 2011, vol. 12, no. 11, pp. 756–766.

    Article  CAS  PubMed  Google Scholar 

  113. Hofreiter, M., Jaenicke, V., Serre, D., Von Haeseler, A., and Pääbo, S., DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA, Nucleic Acid Res., 2001, vol. 29, no. 23, pp. 4793–4799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Hope, A.G., Ho, S.Y.W., Malaney, J.L., Cook, J.A., and Talbot, S.L., Accounting for rate variation among lineages in comparative demographic analyses, Evolution, 2014, vol. 68, no. 9, pp. 2689–2700.

    Article  PubMed  Google Scholar 

  115. Hua, X., Cowman, P., Warren, D., and Bromham, L., Longevity is linked to mitochondrial mutation rates in rockfish: a test using Poisson regression, Mol. Biol. Evol., 2015, vol. 32, no. 10, pp. 2633–2645.

    Article  CAS  PubMed  Google Scholar 

  116. Hua, X. and Bromham, L., Darwinism for the genomic age: connecting mutation to diversification, Front. Genet., 2017, vol. 8. https://doi.org/10.3389/fgene.2017.00012

  117. Huelsenbeck, J.P., Larget, B., and Swofford, D., A compound Poisson process for relaxing the molecular clock, Genetics, 2000, vol. 154, no. 4, pp. 1879–1892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Hug, L.A. and Roger, A.J., The impact of fossils and taxon sampling on ancient molecular dating analyses, Mol. Biol. Evol., 2007, vol. 24, no. 8, pp. 1889–1897.

    Article  CAS  PubMed  Google Scholar 

  119. Igea, J., Aymerich, P., Bannikova, A.A., Gosálbez, J., and Castresana, J., Multilocus species trees and species delimitation in a temporal context: application to the water shrews of the genus Neomys, BMC Evol. Biol., 2015, vol. 15. https://doi.org/10.1186/s12862-015-0485-z

  120. Irwin, D.M., Kocher, T.D., and Wilson, A.C., Evolution of the cytochrome b gene of mammals, J. Mol. Evol., 1991, vol. 32, no. 12, pp. 128–144.

    Article  CAS  PubMed  Google Scholar 

  121. Jarvis, E.D., Mirarab, S., Aberer, A.J., Li, B., Houde, P., et al., Whole-genome analyses resolve early branches in the tree of life of modern birds, Science, 2014, vol. 346, no. 6215, pp. 1320–1331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., Haeseler, A., and Jermiin, L.S., ModelFinder: fast model selection for accurate phylogenetic estimates, Nat. Methods, 2017, vol. 14, no. 6, pp. 587–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kim, S.-H., Elango, N., Warden, C.W., Vigoda, E., and Yi, S., Heterogeneous genomic molecular clocks in primates, PLoS Genet., 2006, vol. 2, no. 10. https://doi.org/10.1371/journal.pgen.0020163

  124. Kimura, M., Evolutionary rate at the molecular level, Nature, 1968, vol. 217, no. 5129, pp. 624–626.

    Article  CAS  PubMed  Google Scholar 

  125. Kimura, M., The rate of molecular evolution considered from the standpoint of population genetics, Proc. Natl. Acad. Sci. USA, 1969, vol. 63, no. 4, pp. 1181–1188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Kimura, M., The Neutral Theory of Molecular Evolution, Cambridge: Cambridge Univ. Press, 1983.

    Book  Google Scholar 

  127. Kimura, M. and Ohta, T., On the rate of molecular evolution, J. Mol. Evol., 1971, vol. 1, no. 1, pp. 1–17.

    Article  CAS  PubMed  Google Scholar 

  128. Kishino, H., Thorne, J.L., and Bruno, W.J., Performance of a divergence time estimation method under a probabilistic model of rate evolution, Mol. Biol. Evol., 2001, vol. 18, no. 3, pp. 352–361.

    Article  CAS  PubMed  Google Scholar 

  129. Kong, A., Frigge, M.L., Masson, G., Besenbacher, S., Sulem, P., et al., Rate of de novo mutations and the importance of father’s age to disease risk, Nature, 2012, vol. 488, no. 7412, pp. 471–475.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Kumar, S., Molecular clocks: four decades of evolution, Nat. Rev. Genet., 2005, vol. 6, no. 8, pp. 654–662.

    Article  CAS  PubMed  Google Scholar 

  131. Kumar, S. and Hedges, S.B., A molecular timescale for vertebrate evolution, Nature, 1998, vol. 392, no. 6679, pp. 917–920.

    Article  CAS  PubMed  Google Scholar 

  132. Kumar, S. and Hedges, S.B., Advances in time estimation methods for molecular data, Mol. Biol. Evol., 2016, vol. 33, no. 4, pp. 863–869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Kumar, S., Filipski, A., Swarna, V., Walker, A., and Hedges, S.B., Placing confidence limits on the molecular age of the human-chimpanzee divergence, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, no. 52, pp. 18842–18847.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Lanfear, R., Thomas, J.A., Welch, J.J., and Bromham, L., Metabolic rate does not calibrate the molecular clock, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, no. 39, pp. 15388–15393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Lanfear, R., Welch, J.J., and Bromham, L., Watching the clock: Studying variation in rates of molecular evolution between species, Trends Ecol. Evol., 2010, vol. 25, no. 9, pp. 495–503.

    Article  PubMed  Google Scholar 

  136. Lanfear, R., Ho, S.Y.W., Davies, T.J., Moles, A.T., Aarssen, L., et al., Taller plants have lower rates of molecular evolution, Nat. Commun., 2013, vol. 4. https://doi.org/10.1038/ncomms2836

  137. Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T., and Calcott, B., Methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses, Mol. Biol. Evol., 2017, vol. 34, no. 3, pp. 772–773.

    CAS  PubMed  Google Scholar 

  138. Langley, C.H. and Fitch, W.M., An estimation of the constancy of the rate of molecular evolution, J. Mol. Evol., 1974, vol. 3, no. 3, pp. 161–177.

    Article  CAS  PubMed  Google Scholar 

  139. Lartillot, N. and Delsuc, F., Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model, Evolution, 2012, vol. 66, no. 6, pp. 1773–1787.

    Article  PubMed  Google Scholar 

  140. Lee, M.S.Y., Molecular clock calibrations and metazoan divergence dates, J. Mol. Evol., 1999, vol. 49, no. 3, pp. 385–391.

    Article  CAS  PubMed  Google Scholar 

  141. Lepage, T., Lawi, S., Tupper, P., and Bryant, D., Continuous and tractable models for the variation of evolutionary rates, Math. Biosci., 2006, vol. 199, no. 2, pp. 216–233.

    Article  PubMed  Google Scholar 

  142. Lopatin, A.V., Early Paleogene insectivore mammals of Asia and establishment of the major groups of Insectivora, Paleontol. J., 2006, vol. 40, no. 3, pp. S205–S405.

    Article  Google Scholar 

  143. Lukoschek, V., Keogh, J.S., and Avise, J.C., Evaluating fossil calibrations for dating phylogenies in light of rates of molecular evolution: a comparison of three approaches, Syst. Biol., 2012, vol. 61, no. 1, pp. 22–43.

    Article  PubMed  Google Scholar 

  144. Lynch, M., Evolution of the mutation rate, Trends Genet., 2010a, vol. 26, no. 8, pp. 345–352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Lynch, M., Rate, molecular spectrum, and consequences of human mutation, Proc. Natl. Acad. Sci. USA, 2010b, vol. 107, no. 3, pp. 961–968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Lynch, M., Ackerman, M.S., Gout, J.-F., Long, H., Sung, W., et al., Genetic drift, selection and the evolution of the mutation rate, Nat. Rev. Genet., 2016, vol. 17, no. 11, pp. 704–714.

    Article  CAS  PubMed  Google Scholar 

  147. Mai, U. and Mirarab, S., Log transformation improves dating of phylogenies, Mol. Biol. Evol., 2021, vol. 38, no. 3, pp. 1151–1167.

    Article  CAS  PubMed  Google Scholar 

  148. Manceau, M., Marin, J., Morlon, H., and Lambert, A., Model-based inference of punctuated molecular evolution, Mol. Biol. Evol., 2020, vol. 37, no. 11, pp. 3308–3323.

    Article  CAS  PubMed  Google Scholar 

  149. Margoliash, E., Primary structure and evolution of cytochrome c, Proc. Natl. Acad. Sci. USA, 1963, vol. 50, no. 4, pp. 672–679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Marshall, C.R., A simple method for bracketing absolute divergence times on molecular phylogenies using multiple fossil calibration points, The American Naturalist, 2008, vol. 171, no. 6, pp. 726–742.

    Article  PubMed  Google Scholar 

  151. Marshall, C.R., Using confidence intervals to quantify the uncertainty in the end-points of stratigraphic ranges, The Paleontological Society Papers, 2010, vol. 16, pp. 291–316.

    Article  Google Scholar 

  152. Martin, A.P. and Palumbi, S.R., Body size, metabolic rate, generation time and the molecular clock, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, no. 9, pp. 4087–4091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Martínková, N., Barnett, R., Cucchi, T., Struchen, R., Pascal, M., et al., Divergent evolutionary processes associated with colonization of offshore islands, Mol. Ecol., 2013, vol. 22, no. 20, pp. 5205–5220.

    Article  PubMed  PubMed Central  Google Scholar 

  154. Matzke, N.J. and Wright, A., Inferring node dates from tip dates in fossil Canidae: the importance of tree priors, Biol. Lett., 2016, vol. 12, no. 8. https://doi.org/10.1098/rsbl.2016.0328

  155. Mayr, E., Animal Species and Evolution, Cambridge: Harvard Univ. Press, 1963.

    Book  Google Scholar 

  156. Mein, P. and Ginsburg, L., Les mammifères du gisement miocène inférieur de Li Mae Long, Thaïlande: systématique, biostratigraphie et paléoenvironnement, Geodiversitas, 1997, vol. 19, no. 4, pp. 783–844.

    Google Scholar 

  157. Mein, P. and Ginsburg, L., Sur l'âge relatif des différents dépôts karstiques miocènes de La Grive-Saint-Alban (Isère), Cahiers Sci. Mus. Hist. Nat. Lyon, 2002, vol. 5, pp. 7–47.

    Google Scholar 

  158. Meredith, R.W., Janecka, J.E., Gatesy, J., Ryder, O.A., Fisher, C.A., et al., Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification, Science, 2011, vol. 334, no. 6055, pp. 521–524.

    Article  CAS  PubMed  Google Scholar 

  159. Milholland, B., Dong, X., Zhang, L., Hao, X., Suh, Y., and Vijg, J., Differences between germline and somatic mutation rates in humans and mice, Nat. Commun., 2017, vol. 8. https://doi.org/10.1038/ncomms15183

  160. Mitchell, K.J., Cooper, A., and Phillips, M.J., Comment on “Whole-genome analyses resolve early branches in the tree of life of modern birds,”” Science, 2015, vol. 349, no. 6255, p. 1460.

    Article  CAS  PubMed  Google Scholar 

  161. Molak, M. and Ho, S.Y.W., Prolonged decay of molecular rate estimates for metazoan mitochondrial DNA, PeerJ, 2015, vol. 3. https://doi.org/10.7717/peerj.821

  162. Mooers, A.O. and Harvey, P.H., Metabolic rate, generation time, and the rate of molecular evolution in birds, Mol. Phylogenet. Evol., 1994, vol. 3, no. 4, pp. 344–350.

    Article  CAS  PubMed  Google Scholar 

  163. Moorjani, P., Amorim, C.E.G., Arndt, P.F., and Przeworski, M., Variation in the molecular clock of primates, Proc. Natl. Acad. Sci. USA, 2016, vol. 113, no. 38, pp. 10607–10612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Müller, H.J., The nature of the genetic effects produced by radiation, in Radiation Biology, New York: McGraw-Hill, 1954, pp. 351–473.

    Google Scholar 

  165. Nabholz, B., Glemin, S., and Galtier, N., Strong variations of mitochondrial mutation rate across mammals-the longevity hypothesis, Mol. Biol. Evol., 2008, vol. 25, no. 1, pp. 120–130.

    Article  CAS  PubMed  Google Scholar 

  166. Nabholz, B., Uwimana, N., and Lartillot, N., Reconstructing the phylogenetic history of long-term effective population size and life-history traits using patterns of amino acid replacement in mitochondrial genomes of mammals and birds, Genome Biol. Evol., 2013, vol. 5, no. 7, pp. 1273–1290.

    Article  PubMed  PubMed Central  Google Scholar 

  167. Nachman, M.W. and Crowell, S.L., Estimate of the mutation rate per nucleotide in humans, Genetics, 2000, vol. 156, no. 1, pp. 297–304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Navascues, M. and Emerson, B.C., Elevated substitution rate estimates from ancient DNA: model violation and bias of Bayesian methods, Mol. Ecol., 2009, vol. 18, no. 21, pp. 4390–4397.

    Article  CAS  PubMed  Google Scholar 

  169. Nei, M., Xu, P., and Glazko, G., Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, no. 5, pp. 2497–2502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Nguyen, J.M.T. and Ho, S.Y.W., Calibrations from the fossil record, in The Molecular Evolutionary Clock, Cham: Springer, 2020, pp. 117–134.

    Google Scholar 

  171. Nunney, L., Lineage selection and the evolution of multistage carcinogenesis, Proc. R. Soc. B, 1999, vol. 266, no. 1418, pp. 493–498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Ogilvie, H.A., Heled, J., Xie, D., and Drummond, A.J., Computational performance and statistical accuracy of *BEAST and comparisons with other methods, Syst. Biol., 2016, vol. 65, no. 3, pp. 381–396.

    Article  PubMed  PubMed Central  Google Scholar 

  173. Ohta, T., Evolutionary rate of cistrons and DNA divergence, J. Mol. Evol., 1972a, vol. 1, no. 2, pp. 150–157.

    Article  CAS  PubMed  Google Scholar 

  174. Ohta, T., Population size and rate of evolution, J. Mol. Evol., 1972b, vol. 1, no. 4, pp. 305–314.

    Article  PubMed  Google Scholar 

  175. Ohta, T., Slightly deleterious mutant substitutions in evolution, Nature, 1973, vol. 246, no. 5428, pp. 96–98.

    Article  CAS  PubMed  Google Scholar 

  176. Ohta, T., Mutational pressure as the main cause of molecular evolution and polymorphism, Nature, 1974, vol. 252, no. 5482, pp. 351–354.

    Article  CAS  Google Scholar 

  177. Ohta, T., Near-neutrality in evolution of genes and gene regulation, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 25, pp. 16134–16137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. O’Leary, M.A., Bloch, J.I., Flynn, J.J., Gaudin, T.J., Giallombardo, A., et al., The placental mammal ancestor and the post-K-Pg radiation of placentals, Science, 2013, vol. 339, no. 6120, pp. 662–667.

    Article  PubMed  Google Scholar 

  179. Pagel, M., Venditti, C., and Meade, A., Large punctuational contribution of speciation to evolutionary divergence at the molecular level, Science, 2006, vol. 314, no. 5796, pp. 119–121.

    Article  CAS  PubMed  Google Scholar 

  180. Pekar, J., Worobey, M., Moshiri, N., Scheffler, K., and Wertheim, J.O., Timing the SARS-CoV-2 index case in Hubei province, Science, 2021, vol. 372, no. 6540, pp. 412–417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Pesole, G., Sbisá, E., Preparata, G., and Saccone, C., The evolution of the mitochondrial D-loop region and the origin of modern man, Mol. Biol. Evol., 1992, vol. 9, no. 4, pp. 587–598.

    CAS  PubMed  Google Scholar 

  182. Peterson, G.I. and Masel, J., Quantitative prediction of molecular clock and Ka/Ks at short timescales, Mol. Biol. Evol., 2009, vol. 26, no. 11, pp. 2595–2603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Pfeifer, S.P., Spontaneous mutation rates, in The Molecular Evolutionary Clock, Cham: Springer, 2020, p. 35–44.

    Google Scholar 

  184. Phillips, M.J., Geomolecular dating and the origin of placental mammals, Syst. Biol., 2016, vol. 65, no. 3, pp. 546–557.

    Article  PubMed  Google Scholar 

  185. Phillips, S.J., Dudík, M., Elith, J., Graham, C.H., Lehmann, A., et al., Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data, Ecological Applications, 2009, vol. 19, no. 1, pp. 181–197.

    Article  PubMed  Google Scholar 

  186. Price, J.P. and Clague, D.A., How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence, Proc. R. Soc. B. Biol. Sci., 2002, vol. 269, no. 1508, pp. 2429–2435.

    Article  Google Scholar 

  187. Qiu, Z.D. and Storch, G., The fossil record of the Eurasian Neogene Insectivores (Erinaceomorpha, Soricomorpha, Mammalia): Part I, Scr. Geol. Spec. Issue. Leiden, 2005, vol. 5, pp. 37–50.

    Google Scholar 

  188. Rambaut, A., Lam, T.T., Carvalho, L.M., and Pybus, O.G., Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen), Virus Evol., 2016, vol. 2, no. 1. https://doi.org/10.1093/ve/vew007

  189. Ramsden, C., Holmes, E.C., and Charleston, M.A., Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence, Mol. Biol. Evol., 2009, vol. 26, no. 1, pp. 143–153.

    Article  CAS  PubMed  Google Scholar 

  190. Rannala, B., Identifiability of parameters in MCMC Bayesian inference of phylogeny, Syst. Biol., 2002, vol. 51, no. 5, pp. 754–760.

    Article  PubMed  Google Scholar 

  191. Rannala, B. and Yang, Z., Inferring speciation times under an episodic molecular clock, Syst. Biol., 2007, vol. 56, no. 3, pp. 453–466.

    Article  PubMed  Google Scholar 

  192. Raspopova, A.A., Bannikova, A.A., and Lebedev, V.S., The phylogeography and demographic history of the common shrew Sorex araneus L., 1758 (Eulipotyphla, Mammalia), Russ. J. Genet., 2018, vol. 54, no. 12, pp. 1452–1465.

    Article  CAS  Google Scholar 

  193. Raspopova, A.A., Bannikova, A.A., Sheftel, B.I., Kryštufek, B., Kouptsov, A.V., et al., A never-ending story of the common shrew: searching for the origin, Mammal. Res., 2020, vol. 65, no. 4, pp. 729–742.

    Article  Google Scholar 

  194. O’Reilly, J.E. and Donoghue, P.C.J., The effect of fossil sampling on the estimation of divergence times with the fossilised birth death process, Syst. Biol., 2020, vol. 69, no. 1, pp. 124–138.

    Article  PubMed  Google Scholar 

  195. Reimer, P.J., Bard, E., Bayliss, A., Beck, J.W., Blackwell, P.G., et al., IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP, Radiocarbon, 2013, vol. 55, no. 4, pp. 1869–1887.

    Article  CAS  Google Scholar 

  196. Rich, T.H.V., Origin and history of the Erinaceidae and Brachyericinae (Mammalia, Insectivora) in North America, Bull. Am. Mus. Nat. Hist., 1981, vol. 171, pp. 1–116.

    Google Scholar 

  197. Ritchie, A.M., Lo, N., and Ho, S.Y., The impact of the tree prior on molecular dating of data sets containing a mixture of inter-and intraspecies sampling, Syst. Biol., 2017, vol. 66, no. 3, pp. 413–425.

    PubMed  Google Scholar 

  198. Roca, A.L., Bar-Gal, G.K., Eizirik, E., Helgen, K.M., Maria, R., et al., Mesozoic origin for west indian insectivores, Nature, 2004, vol. 429, no. 6992, pp. 649–651.

    Article  CAS  PubMed  Google Scholar 

  199. Rodríguez-Trelles, F., Tarrío, R., and Ayala, F.J., A methodological bias toward overestimation of molecular evolutionary time scales, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 12, pp. 8112–8115.

    Article  PubMed  PubMed Central  Google Scholar 

  200. Rogers, A.R. and Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences, Mol. Biol. Evol., 1992, vol. 9, no. 3, pp. 552–569.

    CAS  PubMed  Google Scholar 

  201. Romiguier, J., Ranwez, V., Douzery, E.J.P., and Galtier, N., Genomic evidence for large, long-lived ancestors to placental mammals, Mol. Biol. Evol., 2013, vol. 30, no. 1, pp. 5–13.

    Article  CAS  PubMed  Google Scholar 

  202. Ronquist, F., Klopfstein, S., Vilhelmsen, L., Schulmeister, S., Murray, D.L., and Rasnitsyn, A.P., A total-evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera, Syst. Biol., 2012, vol. 61, no. 6, pp. 973–999.

    Article  PubMed  PubMed Central  Google Scholar 

  203. Sagulenko, P., Puller, V., and Neher, R.A., TreeTime: maximum-likelihood phylodynamic analysis, Virus Evol., 2018, vol. 4, no. 1. https://doi.org/10.1093/ve/vex042

  204. Sanderson, M.J., A nonparametric approach to estimating divergence times in the absence of rate constancy, Mol. Biol. Evol., 1997, vol. 14, no. 12, pp. 1218–1231.

    Article  CAS  Google Scholar 

  205. Sanderson, M.J., Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach, Mol. Biol. Evol., 2002, vol. 19, no. 1, pp. 101–109.

    Article  CAS  PubMed  Google Scholar 

  206. Sanderson, M.J., r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock, Bioinformatics, 2003, vol. 19, no. 2, pp. 301–302.

    Article  CAS  PubMed  Google Scholar 

  207. Santos, C., Montiel, R., Sierra, B., Bettencourt, C., Fernandez, E., et al., Understanding differences between phylogenetic and pedigree-derived mtDNA mutation rate: a model using families from the Azores Islands (Portugal), Mol. Biol. Evol., 2005, vol. 22, no. 6, pp. 1490–1505.

    Article  CAS  PubMed  Google Scholar 

  208. Sarich, V.M. and Wilson, A.C., Immunological time scale for hominid evolution, Science, 1967, vol. 158, no. 3805, pp. 1200–1203.

    Article  CAS  PubMed  Google Scholar 

  209. Scally, A., The mutation rate in human evolution and demographic inference, Curr. Opin. Genet. Dev., 2016, vol. 41, pp. 36–43.

    Article  CAS  PubMed  Google Scholar 

  210. Shapiro, B., Rambaut, A., and Drummond, A.J., Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences, Mol. Biol. Evol., 2006, vol. 23, no. 1, pp. 7–9.

    Article  CAS  PubMed  Google Scholar 

  211. Shapiro, B., Ho, S.Y.W., Drummond, A.J., Suchard, M.A., Pybus, O.G., and Rambaut, A., A Bayesian phylogenetic method to estimate unknown sequence ages, Mol. Biol. Evol., 2011, vol. 28, no. 2, pp. 879–887.

    Article  CAS  PubMed  Google Scholar 

  212. Shenbrot, G., Bannikova, A., Giraudoux, P., Quéré, J.-P., Raoul, F., and Lebedev, V., A new recent genus and species of three-toed jerboas (Rodentia: Dipodinae) from China: a living fossil?, J. Zool. Syst. Evol. Res., 2017, vol. 55, no. 4, pp. 356–368.

    Article  Google Scholar 

  213. Simpson, G.G., The principles of classification and a classification of mammals, Bull. Am. Mus. Nat. Hist., 1945, vol. 85, pp. 1–350.

    Google Scholar 

  214. Smith, A.B. and Peterson, K.J., Dating the time of origin of major clades: Molecular clocks and the fossil record, Annu. Rev. Earth Planet. Sci., 2002, vol. 30, no. 1, pp. 65–88.

    Article  CAS  Google Scholar 

  215. Smith, S.A. and O’Meara, B.C., treepL: divergence time estimation using penalized likelihood for large phylogenies, Bioinformatics, 2012, vol. 28, no. 20, pp. 2689–2690.

    Article  CAS  PubMed  Google Scholar 

  216. Soubrier, J., Steel, M., Lee, M.S.Y., Der Sarkissian, C., Guindon, S., et al., The influence of rate heterogeneity among sites on the time dependence of molecular rates, Mol. Biol. Evol., 2012, vol. 29, no. 11, pp. 3345–3358.

    Article  CAS  PubMed  Google Scholar 

  217. Springer, M.S., Murphy, W.J., Eizirik, E., and O’Brien, S.J., Placental mammal diversification and the Cretaceous-Tertiary boundary, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, no. 3, pp. 1056–1062.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Springer, M.S., Meredith, R.W., Gatesy, J., Emerling, C.A., Park, J., et al., Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix, PLoS One, 2012, vol. 7, no. 11. https://doi.org/10.1371/journal.pone.0049521

  219. Springer, M.S., Emerling, C.A., Meredith, R.W., Janečka, J.E., Eizirik, E., and Murphy, W.J., Waking the undead: implications of a soft explosive model for the timing of placental mammal diversification, Mol. Phylogenet. Evol., 2017, vol. 106, pp. 86–102.

    Article  PubMed  Google Scholar 

  220. Stadler, T., Kühnert, D., Bonhoeffer, S., and Drummond, A.J., Birth-death skyline plot reveals temporal changes of epidemic spread in HIV and hepatitis C virus (HCV), Proc. Natl. Acad. Sci. USA, 2013, vol. 110, no. 1, pp. 228–233.

    Article  CAS  PubMed  Google Scholar 

  221. Stadler, T., Sampling-through-time in birth-death trees, J. Theor. Biol., 2010, vol. 267, no. 3, pp. 396–404.

    Article  PubMed  Google Scholar 

  222. Stebbins, G.L. and Lewontin, R.C., Comparative evolution at the levels of molecules, organisms, and populations, in Darwinian, Neo-Darwinian, and Non-Darwinian Evolution, Berkeley: Univ. California Press, 1972, pp. 23–42.

    Google Scholar 

  223. Storch, G. and Qiu, S., Insectivores (Mammalia: Erinaceidae, Soricidae, Talpidae) from the Lufeng hominoid locality, Late Miocene of China, Geobios, 1991, vol. 24, no. 5, pp. 601–621.

    Article  Google Scholar 

  224. Suzuki, M. and Bird, A., DNA methylation landscapes: provocative insights from epigenomics, Nat. Rev. Genet., 2008, vol. 9, no. 6, pp. 465–476.

    Article  CAS  PubMed  Google Scholar 

  225. Tajima, F., Simple methods for testing the molecular evolutionary clock hypothesis, Genetics, 1993, vol. 135, no. 2, pp. 599–607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Takezaki, N., Rzhetsky, A., and Nei, M., Phylogenetic test of the molecular clock and linearized trees, Mol. Biol. Evol., 1995, vol. 12, no. 5, pp. 823–833.

    CAS  PubMed  Google Scholar 

  227. Tamura, K., Battistuzzi, F.U., Billing-Ross, P., Murillo, O., Filipski, A., and Kumar, S., Estimating divergence times in large molecular phylogenies, Proc. Natl. Acad. Sci. USA, 2012, vol. 109, no. 47, pp. 19333–19338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Tamura, K., Tao, Q., and Kumar, S., Theoretical foundation of the RelTime method for estimating divergence times from variable evolutionary rates, Mol. Biol. Evol., 2018, vol. 35, no. 7, pp. 1170–1182.

    Article  Google Scholar 

  229. Tao, Q., Tamura, K., Battistuzzi, F.U., and Kumar, S., A machine learning method for detecting autocorrelation of evolutionary rates in large phylogenies, Mol. Biol. Evol., 2019, vol. 36, no. 4, pp. 811–824.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  230. Thomas, J.A., Welch, J.J., Lanfear, R., and Bromham, L., A generation time effect on the rate of molecular evolution in invertebrates, Mol. Biol. Evol., 2010, vol. 27, no. 5, pp. 1173–1180.

    Article  CAS  PubMed  Google Scholar 

  231. Thorne, J.L., Kishino, H., and Painter, I.S., Estimating the rate of evolution of the rate of molecular evolution, Mol. Biol. Evol., 1998, vol. 15, no. 12, pp. 1647–1657.

    Article  CAS  PubMed  Google Scholar 

  232. To, T.-H., Jung, M., Lycett, S., and Gascuel, O., Fast dating using least-squares criteria and algorithms, Syst. Biol., 2016, vol. 65, no. 1, pp. 82–97.

    Article  CAS  PubMed  Google Scholar 

  233. Tong, K.J., Lo, N., and Ho, S.Y.W., Reconstructing evolutionary timescales using phylogenomics, Zool. Syst., 2016, vol. 41, no. 4, pp. 343–351.

    Google Scholar 

  234. Tuffley, C., Timothy, W., White, J., Hendy, M.D., and Penny, D., Correcting the apparent mutation rate acceleration at shorter time scales under a Jukes-Cantor model, Mol. Biol. Evol., 2012, vol. 29, no. 12, pp. 3703–3709.

    Article  CAS  PubMed  Google Scholar 

  235. Vandiver, A.R., Idrizi, A., Rizzardi, L., Feinberg, A.P., and Hansen, K.D., DNA methylation is stable during replication and cell cycle arrest, Sci. Rep., 2015, vol. 5. https://doi.org/10.1038/srep17911

  236. Volz, E.M. and Frost, S.D.W., Scalable relaxed clock phylogenetic dating, Virus Evol., 2017, vol. 3, no. 2. https://doi.org/10.1093/ve/vex025

  237. Warnock, R.C.M., Parham, J.F., Joyce, W.G., Lyson, T.R., and Donoghue, P.C.J., Calibration uncertainty in molecular dating analyses: there is no substitute for the prior evaluation of time priors, Proc. R. Soc. B. Biol. Sci., 2015, vol. 282, no. 1798. https://doi.org/10.1098/rspb.2014.1013

  238. Webster, A.J., Payne, R.J.H., and Pagel, M., Molecular phylogenies link rates of evolution and speciation, Science, 2003, vol. 301, no. 5632, p. 478.

    Article  CAS  PubMed  Google Scholar 

  239. Welch, J.J. and Bromham, L., Molecular dating when rates vary, Trends Ecol. Evol., 2005, vol. 20, no. 6, pp. 320–327.

    Article  PubMed  Google Scholar 

  240. Welch, J.J., Bininda-Emonds, O.R., and Bromham, L., Correlates of substitution rate variation in mammalian protein-coding sequences, BMC Evol. Biol., 2008, vol. 8. https://doi.org/10.1186/1471-2148-8-53

  241. Weller, C. and Wu, M., A generation-time effect on the rate of molecular evolution in bacteria, Evolution, 2015, vol. 69, no. 3, pp. 643–652.

    Article  CAS  PubMed  Google Scholar 

  242. Wilson Sayres, M.A. and Makova, K.D., Genome analyses substantiate male mutation bias in many species, BioEssays, 2011, vol. 33, no. 12, pp. 938–945.

    Article  PubMed  Google Scholar 

  243. Wilson, A.C., Carlson, S.S., and White, T.J., Biochemical evolution, Annu. Rev. Biochem., 1977, vol. 46, no. 1, pp. 573–639.

    Article  CAS  PubMed  Google Scholar 

  244. Wilson, A.C., Cann, R.L., Carr, S.M., George, M., Gyllensten, U.B., et al., Mitochondrial DNA and two perspectives on evolutionary genetics, Biol. J. Linn. Soc., 1985, vol. 26, no. 4, pp. 375–400.

    Article  Google Scholar 

  245. Woodhams, M., Can deleterious mutations explain the time dependency of molecular rate estimates?, Mol. Biol. Evol., 2006, vol. 23, no. 12, pp. 2271–2273.

    Article  CAS  PubMed  Google Scholar 

  246. Wu, C.I. and Li, W.H., Evidence for higher rates of nucleotide substitution in rodents than in man, Proc. Natl. Acad. Sci. USA, 1985, vol. 82, no. 6, pp. 1741–1745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Yang, Z. and Rannala, B., Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds, Mol. Biol. Evol., 2006, vol. 23, no. 1, pp. 212–226.

    Article  CAS  PubMed  Google Scholar 

  248. Yoder, A.D. and Yang, Z., Estimation of primate speciation dates using local molecular clocks, Mol. Biol. Evol., 2000, vol. 17, no. 7, pp. 1081–1090.

    Article  CAS  PubMed  Google Scholar 

  249. Zheng, Y. and Wiens, J.J., Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species, Mol. Phylogenet. Evol., 2016, vol. 94, pp. 537–547.

    Article  PubMed  Google Scholar 

  250. Zhu, T., Bayesian molecular dating, in The Molecular Evolutionary Clock, Cham: Springer, 2020, pp. 83–100.

    Google Scholar 

  251. Zhu, T., Dos Reis, M., and Yang, Z., Characterization of the uncertainty of divergence time estimation under relaxed molecular clock models using multiple loci, Syst. Biol., 2015, vol. 64, no. 2, pp. 267–280.

    Article  CAS  PubMed  Google Scholar 

  252. Zuckerkandl, E. and Pauling, L., Molecular disease, evolution, and genic heterogeneity, in Horizons in Biochemistry, Kasha, M. and Pullman, B.N., Eds., New York: Academic Press, 1962, pp. 189–225.

    Google Scholar 

  253. Zuckerkandl, E. and Pauling, L., Evolutionary divergence and convergence in proteins, in Evolving Genes and Proteins, New York: Academic Press, 1965, pp. 97–166.

    Google Scholar 

Download references

Funding

The study was supported by the Russian Foundation for Basic Research, project no. 20-14-50062.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to A. A. Bannikova or V. S. Lebedev.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Makeeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bannikova, A.A., Lebedev, V.S. The Concept of the Modern Molecular Clock and Experience in Estimating Divergence Times of Eulipotyphla and Rodentia. Biol Bull Rev 12, 459–482 (2022). https://doi.org/10.1134/S2079086422050024

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086422050024

Navigation