Abstract
The best reconstructions of the history of life will use both molecular time estimates and fossil data. Errors in molecular rate estimation typically are unaccounted for and no attempts have been made to quantify this uncertainty comprehensively. Here, focus is primarily on fossil calibration error because this error is least well understood and nearly universally disregarded. Our quantification of errors in the synapsid–diapsid calibration illustrates that although some error can derive from geological dating of sedimentary rocks, the absence of good stem fossils makes phylogenetic error the most critical. We therefore propose the use of calibration ages that are based on the first undisputed synapsid and diapsid. This approach yields minimum age estimates and standard errors of 306.1 ± 8.5 MYR for the divergence leading to birds and mammals. Because this upper bound overlaps with the recent use of 310 MYR, we do not support the notion that several metazoan divergence times are significantly overestimated because of serious miscalibration (sensu Lee 1999). However, the propagation of relevant errors reduces the statistical significance of the pre-K–T boundary diversification of many bird lineages despite retaining similar point time estimates. Our results demand renewed investigation into suitable loci and fossil calibrations for constructing evolutionary timescales.
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References
BS Arbogast JB Slowinski (1998) ArticleTitlePleistocene speciation and the mitochondrial clock Science 282 1955a
BS Arbogast SV Edwards J Wakeley P Beerli JB Slowinski (2002) ArticleTitleEstimating divergence times from molecular data on phylogenetic and population genetic timescales Annu Rev Ecol Syst 33 707–740
WA Bell (1966) ArticleTitleCarboniferous rocks and fossil floras of northern Nova Scotia Can Geol Surv Memoir 238 1–277
MJ Benton (1990) ArticleTitlePhylogeny of the major tetrapod groups: morphological data and divergence dates J Mol Evol 30 409–424 Occurrence Handle1:STN:280:By%2BB28vpsVw%3D Occurrence Handle2111854
MJ Benton (1993) The fossil record 2. Chapman & Hall London
MJ Benton (1997) Vertebrate paleontology, EditionNumber 2nd ed. Chapman & Hall London
MJ Benton (1999) ArticleTitleEarly origins of modern birds and mammals: Molecules vs. morphology Bioessays 21 1043–1051 Occurrence Handle1:STN:280:DC%2BD3c%2FkslOhsw%3D%3D Occurrence Handle10580989
MJ Benton F Ayala (2003) ArticleTitleDating the tree of life Science 5626 1698–1700
R Bleiweiss (1998) ArticleTitleSlow rate of molecular evolution in high-elevation hummingbirds Proc Natl Acad Sci USA 95 612–616 Occurrence Handle1:CAS:528:DyaK1cXmtFajsw%3D%3D Occurrence Handle9435240
L Bromham (2002) ArticleTitleMolecular clocks in reptiles: Life history influences rate of molecular evolution Mol Biol Evol 19 302–309 Occurrence Handle1:CAS:528:DC%2BD38XitFSnsLo%3D Occurrence Handle11861889
L Bromham A Rambaut PH Harvey (1996) ArticleTitleDeterminants of rate variation in mammalian DNA sequence evolution J Mol Evol 43 610–621 Occurrence Handle1:CAS:528:DyaK2sXislKjtg%3D%3D Occurrence Handle8995058
WM Brown M George SuffixJr AC Wilson (1979) ArticleTitleRapid evolution of animal mitochondrial DNA Proc Natl Acad Sci USA 67 1967–1971
F Bossuyt MC Milinkovitch (2001) ArticleTitleAmphibians as indicators of early Tertiary “out-of-India” dispersal of vertebrates Science 292 93–95 Occurrence Handle1:CAS:528:DC%2BD3MXis1Grtrs%3D Occurrence Handle11292870
TR Buckley C Simon GK Chambers (2001) ArticleTitleExploring among-site rate variation models in a maximum likelihood framework using empirical data: Effects of model assumptions on estimates of topology, branch lengths, and bootstrap support Syst Biol 50 67–86 Occurrence Handle1:STN:280:DC%2BD38zntVOhtw%3D%3D Occurrence Handle12116595
JH Calder (1994) ArticleTitleThe impact of climate change, tectonism and hydrology on the formation of Carboniferous tropical intermontane mires: The Springhill coalfield, Cumberland Basin, Nova Scotia Palaeogeogr Palaeoclimat Palaeoecol 106 323–351
RL Carroll (1964) ArticleTitleThe earliest reptiles J Linn Soc Zool 45 61–83
RL Carroll (1970) ArticleTitleThe ancestry of reptiles Philos Trans R Soc Lond B 257 267–308
RL Carroll (1988) Vertebrate paleontology and evolution. Freeman New York
RL Carroll (1991) The origin of reptiles HP Schultze L Trueb (Eds) Origins of the higher groups of tetrapods: Controversy and consensus Cornell University Press Ithaca, NY 331–354
RL Carroll (1995) ArticleTitlePhylogenetic analysis of Paleozoic choanates Bull Mus Nat Hist Nat Paris 17 389–445
RL Carroll (2001) ArticleTitleThe origin and early radiation of terrestrial vertebrates J Paleo 75 1202–1213
Claoué-Long JC, Compston W, Roberts J, Fanning CM (1995) Two Carboniferous ages: a comparison of SHRIMP zircon dating with conventional zircon ages and 40Ar/39Ar analyses. In: Berggren WA, Kent DV, Aubry M-P, Hardenbol JA (eds) Geochronology, time scales, and global stratigraphic correlations: A unified temporal framework for an historical geology. Soc Econ Geol Mineral, Tulsa, OK, 54, pp 3–21
J Clark RL Carroll (1973) ArticleTitleRomeriid reptiles from the Lower Permian Bull Mus Comp Zool Harvard Univ 144 353–407
A Cooper DP Penny (1997) ArticleTitleMass survival of birds across the Cretaceous–Tertiary: Molecular evidence Science 275 1109–1113
JW Dawson Sir (1891) Acadian geology. EditionNumber4 Macmillan London
RF Doolittle DF Feng S Tsang G Cho E Little (1996) ArticleTitleDetermining divergence times of the major kingdoms of living organisms with a protein clock Science 271 470–477 Occurrence Handle1:CAS:528:DyaK28XmvFyktg%3D%3D Occurrence Handle8560259
S Easteal C Collet D Betty (1995) The mammalian molecular clock. Springer Verlag Heidelberg, Germany
PH Heckel (1975) ArticleTitleStratigraphy and depositional framework of the Stanton Formation in Southeastern Kansas Kans Geol Bull 210 1–45
SB Hedges (2002) ArticleTitleThe origin of evolution of model organisms Nat Rev Gen 3 838–849 Occurrence Handle1:CAS:528:DC%2BD38Xotlersbo%3D
SB Hedges S Kumar (2003) ArticleTitleGenomic clocks and evolutionary timescales TIG 19 200–206 Occurrence Handle12683973
SB Hedges PH Parker CG Sibley S Kumar (1996) ArticleTitleContinental breakup and the ordinal diversification of birds and mammals Nature 381 226–229 Occurrence Handle10.1038/381226a0 Occurrence Handle1:CAS:528:DyaK28XjtVKiu7o%3D Occurrence Handle8622763
JC Hess HJ Lippolt (1986) ArticleTitle40Ar/39Ar ages of tonstein and tuff sandines: new calibration points for the improvement of the Upper Carboniferous time scale Chem Geol 59 143–154 Occurrence Handle1:CAS:528:DyaL2sXltlGrsg%3D%3D
SP Hesselbo NH Trewin (1984) ArticleTitleDeposition, diagenesis and structures of the Cheese Bay Shrimp Bed, Lower Carboniferous, East Lothian Scott J Geol 20 281–296
DM Hillis BK Mable C Moritz et al. (1997) Applications of molecular systematics DM Hillis (Eds) Molecular systematics Sinauer Associates Sunderland, MA 515–544
A Janke U Arnason (1997) ArticleTitleThe complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles) Mol Biol Evol 14 1266–1272 Occurrence Handle1:CAS:528:DyaK2sXnvVGiurk%3D Occurrence Handle9402737
M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences J Mol Evol 16 111–120 Occurrence Handle1:CAS:528:DyaL3MXmtFSktg%3D%3D Occurrence Handle7463489
S Kumar SB Hedges (1998) ArticleTitleA molecular timescale for vertebrate evolution Nature 392 917–919 Occurrence Handle10.1038/31927 Occurrence Handle1:CAS:528:DyaK1cXjtV2jur8%3D Occurrence Handle9582070
S Kumar S Subramanian (2002) ArticleTitleMutation rates in mammalian genomes Proc Natl Acad Sci USA 99 803–808 Occurrence Handle1:CAS:528:DC%2BD38Xht1Wis74%3D Occurrence Handle11792858
M Laurin RR Reisz (1995) ArticleTitleA reevaluation of early amniote phylogeny Zool J Linn Soc 113 165–223
M Laurin RR Reisz (1997) A new perspective on tetrapod phylogeny SS Sumida KLM Martin (Eds) Amniote origins: Completing the transition to land Academic Press San Diego 9–59
MSY Lee (1999) ArticleTitleMolecular clock calibrations and metazoan divergence dates J Mol Evol 49 385–391 Occurrence Handle1:CAS:528:DyaK1MXmtlGksbo%3D Occurrence Handle10473780
CR Marshall (1990) ArticleTitleThe fossil record and estimating divergence times between lineages: Maximum divergence times and the importance of reliable phylogenies J Mol Evol 30 400–408 Occurrence Handle1:STN:280:By%2BB28vpsVM%3D Occurrence Handle2111853
E Margoliash E Smith (1965) Structural and functional aspects of cytochrome c in relation to evolution V Bryson HJ Vogel (Eds) Evolving genes and proteins Academic Press New York 221–242
M Menning D Weyer G Drozdzewski HWJ Amerom Particlevan I Wendt (2000) ArticleTitleA Carboniferous timescale 2000: Discussion and use of geological parameters as time indicators from Central and (Western Europe) Geol Jahrb A 156 3–44
AR Milner (1987) ArticleTitleThe Westphalian tetrapod fauna: some aspects of its geography and ecology J Geol Soc Lond 144 495–506
R Moussavi-Harami (1990) ArticleTitleStratigraphy, petrology, and depositional environment of sandstones in the Rock Lake Shale member of the Stanton Limestone (Missourian stage, Upper Pennsylvanian) in Southeastern Kansas Kans Geol Surv 5 1–44
M Nei S Kumar (2000) Molecular clocks and linearized trees M Nei S Kumar (Eds) Molecular evolution and phylogenetics Oxford University Press New York 187–206
M Nei P Xu G Glazko (2001) ArticleTitleEstimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms Proc Natl Acad Sci USA 98 2497–2502 Occurrence Handle10.1073/pnas.051611498 Occurrence Handle1:CAS:528:DC%2BD3MXhslKmsrc%3D Occurrence Handle11226267
GB Nunn SE Stanley (1998) ArticleTitleBody size effects and rates of cytochrome b evolution in tube-nosed seabirds Mol Biol Evol 15 1360–1371 Occurrence Handle1:CAS:528:DyaK1cXms1eks7c%3D Occurrence Handle9787440
T Ohta JH Gillespie (1996) ArticleTitleDevelopment of neutral and nearly neutral theories Theor Pop Biol 49 128–142
RL Paton TR Smithson JA Clack (1999) ArticleTitleAn amniote-like skeleton from the Early Carboniferous of Scotland Nature 398 508–513 Occurrence Handle1:CAS:528:DyaK1MXisFGqt74%3D
T Paton O Haddrath AJ Baker (2001) ArticleTitleComplete mitochondrial DNA genome sequences show that modern birds are not descended from transitional shorebirds Proc R Soc Lond B 269 839–846
TA Paton AJ Baker JG Groth GF Barrowclough (2003) ArticleTitleRAG-1 sequences resolve the phylogenetic relationships within Charadriiform birds Mol Phylogenet Evol 29 268–278 Occurrence Handle1:CAS:528:DC%2BD3sXnt1amtrw%3D Occurrence Handle13678682
A Rambaut L Bromham (1998) ArticleTitleEstimating divergence dates from molecular sequences Mol Biol Evol 15 442–448 Occurrence Handle1:CAS:528:DyaK1cXitlKiu70%3D Occurrence Handle9549094
RR Reisz (1972) ArticleTitlePelycosaurian reptiles from the Middle Pennsylvanian of North America Bull Mus Comp Zool Harvard Univ 144 27–62
RR Reisz (1977) ArticleTitlePetrolacosaurus, the oldest known diapsid reptile Science 196 1091–1093
RR Reisz (1981) ArticleTitleA diapsid reptile from the Pennsylvanian of Kansas Special Publ Mus Nat Hist Univ Kans 7 1–74
RR Reisz (1997) ArticleTitleThe origin and early evolutionary history of amniotes TREE 12 218–222
RR Reisz MJ Heaton B Pynn (1982) ArticleTitleVertebrate fauna of late Pennsylvanian rock lake shale near Garnett, Kansas: Pelycosauria J Paleo 56 741–750
Rolfe WDI, Clarkson ENK, Panchen AL (eds) (1993) Volcanism and early terrestrial biotas, Trans R Soc Edinburgh Earth Sci 84, parts 3 and 4
MJ Sanderson (1997) ArticleTitleA nonparametric approach to estimating divergence times in the absence of rate constancy Mol Biol Evol 14 1218–1231 Occurrence Handle1:CAS:528:DyaK2sXnvVCrsbk%3D
SG Shapiro (1991) ArticleTitleUniformity in the nonsynonymous substitution rates of embryonic beta-globin of several vertebrate species J Mol Evol 32 122–127 Occurrence Handle1:CAS:528:DyaK3MXhtFKitb8%3D Occurrence Handle1901091
TR Smithson (1989) ArticleTitleThe earliest known reptile Nature 342 676–678
TR Smithson RL Carroll AL Panchen SM Andrews (1993) ArticleTitleWestlothiana lizziae from the Viséan of East Kirkton, West Lothian, Scotland, and the amniote stem Trans R Soc Edinburgh Earth Sci 84 383–412
SS Sumida (1997) Locomotor features of taxa spanning the origin of amniotes SS Sumida KLM Martin (Eds) Amniote origins: Completing the transition to land Academic Press San Diego 353–398
JGM Thewissen EM Williams LJ Roe ST Hussain (2001) ArticleTitleSkeletons of terrestrial Cetaceans and the relationship of whales to artiodactyls Nature 413 277–281 Occurrence Handle1:CAS:528:DC%2BD3MXnt1Kisrs%3D Occurrence Handle11565023
JL Thorne H Kishino IS Painter (1998) ArticleTitleEstimating the rate of evolution of the rate of molecular evolution Mol Biol Evol 15 1647–1657 Occurrence Handle1:CAS:528:DyaK1MXjtVOk Occurrence Handle9866200
M Tuinen Particlevan SB Hedges (2001) ArticleTitleCalibration of avian molecular clocks Mol Biol Evol 18 206–213 Occurrence Handle11158379
M Tuinen Particlevan SB Hedges (2004) ArticleTitleThe effect of external and internal fossil calibrations on the avian evolutionary timescale J Paleo 78 45–50
AC Wilson SS Carlson TJ White (1977) ArticleTitleBiochemical evolution Annu Rev Biochem 46 573–639 Occurrence Handle1:CAS:528:DyaE2sXltFehsrY%3D Occurrence Handle409339
E Zuckerkandl L Pauling (1965) Evolutionary divergence and convergence in proteins V Bryson HJ Vogel (Eds) Evolving genes and proteins Academic Press New York 97–166
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For valuable comments we thank Robert Reisz, Hans Thewissen, Blair Hedges, Susan Holmes, Stephen Porder, three anonymous reviewers, and members of the Hadly lab.
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van Tuinen, M., Hadly, E.A. Error in Estimation of Rate and Time Inferred from the Early Amniote Fossil Record and Avian Molecular Clocks. J Mol Evol 59, 267–276 (2004). https://doi.org/10.1007/s00239-004-2624-9
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DOI: https://doi.org/10.1007/s00239-004-2624-9