{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,13]],"date-time":"2026-03-13T03:01:00Z","timestamp":1773370860817,"version":"3.50.1"},"reference-count":129,"publisher":"Wiley","issue":"8","license":[{"start":{"date-parts":[[2001,8,1]],"date-time":"2001-08-01T00:00:00Z","timestamp":996624000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["DEB\u20109726856"],"award-info":[{"award-number":["DEB\u20109726856"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["American J of Botany"],"published-print":{"date-parts":[[2001,8]]},"abstract":"<jats:p>Molecular estimates of the age of angiosperms have varied widely, and many greatly predate the Early Cretaceous appearance of angiosperms in the fossil record, but there have been few attempts to assess confidence limits on ages. Experiments with <jats:italic>rbcL<\/jats:italic> and 18S data using maximum likelihood suggest that previous angiosperm age estimates were too old because they assumed equal rates across sites\u2014use of a gamma distribution of rates to correct for site\u2010to\u2010site variation gives 10\u201330 my (million years) younger ages\u2014and relied on herbaceous angiosperm taxa with high rates of molecular evolution. Ages based on first and second codon positions of <jats:italic>rbcL<\/jats:italic> are markedly older than those based on third positions, which conflict with the fossil record in being too young, but all examined data partitions of <jats:italic>rbcL<\/jats:italic> and 18S depart substantially from a molecular clock. Age estimates are surprisingly insensitive to different views on seed\u2010plant relationships. Randomization schemes were used to quantify confidence intervals due to phylogenetic uncertainty, substitutional noise, and lineage effects (deviations from a molecular clock). Estimates of the age of crown\u2010group angiosperms range from 68 to 281 mya (million years ago), depending on data, tree, and assumptions, with most \u223c140\u2013190 mya (Early Jurassic\u2013earliest Cretaceous). Approximate 95% confidence intervals on ages are wider for <jats:italic>rbcL<\/jats:italic> than 18S, ranging up to 160 my for phylogenetic uncertainty, 90 my for substitutional noise, and 70 my for lineage effects. These intervals overlap the oldest occurrences of angiosperms in the fossil record, as well as some estimates from previous molecular studies.<\/jats:p>","DOI":"10.2307\/3558458","type":"journal-article","created":{"date-parts":[[2007,2,2]],"date-time":"2007-02-02T17:42:15Z","timestamp":1170438135000},"page":"1499-1516","source":"Crossref","is-referenced-by-count":200,"title":["Sources of error and confidence intervals in estimating the age of angiosperms from <i>rbcL<\/i> and 18S rDNA data"],"prefix":"10.1002","volume":"88","author":[{"given":"Michael J.","family":"Sanderson","sequence":"first","affiliation":[]},{"given":"James A.","family":"Doyle","sequence":"additional","affiliation":[]}],"member":"311","published-online":{"date-parts":[[2001,8]]},"reference":[{"key":"e_1_2_5_2_1","doi-asserted-by":"publisher","DOI":"10.2307\/2399902"},{"key":"e_1_2_5_3_1","doi-asserted-by":"publisher","DOI":"10.2307\/2992015"},{"key":"e_1_2_5_4_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4615-2381-9"},{"key":"e_1_2_5_5_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.1952.tb02810.x"},{"key":"e_1_2_5_6_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02858880"},{"key":"e_1_2_5_7_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.94.15.7776"},{"key":"e_1_2_5_8_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.16.9402"},{"key":"e_1_2_5_9_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.220427497"},{"key":"e_1_2_5_10_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.89.16.7844"},{"key":"e_1_2_5_11_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.97.8.4092"},{"key":"e_1_2_5_12_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1992.0077"},{"key":"e_1_2_5_13_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-0-585-23095-5_5"},{"key":"e_1_2_5_14_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.3082006"},{"key":"e_1_2_5_15_1","doi-asserted-by":"publisher","DOI":"10.1007\/s002399910034"},{"key":"e_1_2_5_16_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4757-2917-7"},{"key":"e_1_2_5_17_1","doi-asserted-by":"publisher","DOI":"10.2307\/2399846"},{"key":"e_1_2_5_18_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.97.8.4086"},{"key":"e_1_2_5_19_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a025702"},{"key":"e_1_2_5_20_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.91.15.6795"},{"key":"e_1_2_5_21_1","doi-asserted-by":"publisher","DOI":"10.2307\/2399221"},{"key":"e_1_2_5_22_1","doi-asserted-by":"publisher","DOI":"10.1086\/297403"},{"key":"e_1_2_5_23_1","doi-asserted-by":"publisher","DOI":"10.1038\/342131b0"},{"key":"e_1_2_5_24_1","doi-asserted-by":"publisher","DOI":"10.1038\/374027a0"},{"key":"e_1_2_5_25_1","doi-asserted-by":"publisher","DOI":"10.2307\/2419407"},{"key":"e_1_2_5_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-9822(00)00304-3"},{"key":"e_1_2_5_27_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4615-3276-7_15"},{"key":"e_1_2_5_28_1","doi-asserted-by":"publisher","DOI":"10.5962\/bhl.part.24686"},{"key":"e_1_2_5_29_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.es.09.110178.002053"},{"key":"e_1_2_5_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/0195-6671(92)90039-S"},{"key":"e_1_2_5_31_1","doi-asserted-by":"publisher","DOI":"10.1086\/297401"},{"key":"e_1_2_5_32_1","doi-asserted-by":"publisher","DOI":"10.1006\/mpev.1998.0506"},{"key":"e_1_2_5_33_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ecolsys.29.1.567"},{"key":"e_1_2_5_34_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02861082"},{"key":"e_1_2_5_35_1","doi-asserted-by":"publisher","DOI":"10.1017\/S0094837300015840"},{"key":"e_1_2_5_36_1","doi-asserted-by":"publisher","DOI":"10.2307\/2399899"},{"key":"e_1_2_5_37_1","first-page":"139","volume-title":"Origin and early evolution of angiosperms","author":"Doyle J.A.","year":"1976"},{"key":"e_1_2_5_38_1","first-page":"A","article-title":"Reconciling fossil and molecular evidence on the age of the angiosperms","volume":"32","author":"Doyle J.A.","year":"2000","journal-title":"Geological Society of America Abstracts with Programs"},{"key":"e_1_2_5_39_1","doi-asserted-by":"publisher","DOI":"10.1086\/337838"},{"key":"e_1_2_5_40_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a025781"},{"key":"e_1_2_5_41_1","doi-asserted-by":"publisher","DOI":"10.2307\/2413663"},{"key":"e_1_2_5_42_1","doi-asserted-by":"publisher","DOI":"10.2307\/2412923"},{"key":"e_1_2_5_43_1","doi-asserted-by":"publisher","DOI":"10.1086\/284325"},{"key":"e_1_2_5_44_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ge.22.120188.002513"},{"key":"e_1_2_5_45_1","author":"Felsenstein J.","year":"1993","journal-title":"PHYLIP: phylogenetic inference package"},{"key":"e_1_2_5_46_1","first-page":"160","volume-title":"Molecular evolution","author":"Fitch W.M.","year":"1976"},{"key":"e_1_2_5_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/0034-6667(83)90015-5"},{"key":"e_1_2_5_48_1","first-page":"1","article-title":"Reproductive structures of Cretaceous Platanaceae","volume":"31","author":"Friis E.M.","year":"1988","journal-title":"Biologiske Skrifter Danske Videnskabernes Selskab"},{"key":"e_1_2_5_49_1","first-page":"145","volume-title":"The origins of angiosperms and their biological consequences","author":"Friis E.M.","year":"1987"},{"key":"e_1_2_5_50_1","doi-asserted-by":"publisher","DOI":"10.1086\/297217"},{"key":"e_1_2_5_51_1","first-page":"31","article-title":"Angiosperm floral structures from the Early Cretaceous of Portugal","volume":"8","author":"Friis E.M.","year":"1994","journal-title":"Plant Systematics and Evolution"},{"key":"e_1_2_5_52_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00161167"},{"key":"e_1_2_5_53_1","doi-asserted-by":"publisher","DOI":"10.1006\/mpev.1993.1009"},{"key":"e_1_2_5_54_1","first-page":"620","article-title":"Detecting substitution\u2010rate heterogeneity among regions of a nucleotide sequence","volume":"11","author":"Gaut B. S.","year":"1994","journal-title":"Molecular Biology and Evolution"},{"key":"e_1_2_5_55_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.es.17.110186.003225"},{"key":"e_1_2_5_56_1","volume-title":"The causes of molecular evolution","author":"Gillespie J.H.","year":"1991"},{"key":"e_1_2_5_57_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a025597"},{"key":"e_1_2_5_58_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00987956"},{"key":"e_1_2_5_59_1","doi-asserted-by":"publisher","DOI":"10.2307\/2656749"},{"key":"e_1_2_5_60_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4615-3276-7_4"},{"key":"e_1_2_5_61_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a026176"},{"key":"e_1_2_5_62_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.en.10.010165.000525"},{"key":"e_1_2_5_63_1","first-page":"1","volume-title":"Monocotyledons: systematics and evolution","author":"Herendeen P. S.","year":"1995"},{"key":"e_1_2_5_64_1","first-page":"515","volume-title":"Molecular systematics","author":"Hillis D. M.","year":"1996"},{"key":"e_1_2_5_65_1","doi-asserted-by":"publisher","DOI":"10.1093\/genetics\/154.4.1879"},{"key":"e_1_2_5_66_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.276.5310.227"},{"key":"e_1_2_5_67_1","volume-title":"The enigma of angiosperm origins","author":"Hughes N.F.","year":"1994"},{"key":"e_1_2_5_68_1","first-page":"443","volume-title":"The origin of major invertebrate groups","author":"Jefferies R.P.S.","year":"1979"},{"key":"e_1_2_5_69_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00985205"},{"key":"e_1_2_5_70_1","doi-asserted-by":"publisher","DOI":"10.2307\/2446015"},{"key":"e_1_2_5_71_1","doi-asserted-by":"publisher","DOI":"10.1016\/0025-5564(95)00083-6"},{"key":"e_1_2_5_72_1","volume-title":"The origin and early diversification of land plants: a cladistic study","author":"Kenrick P. P.","year":"1997"},{"key":"e_1_2_5_73_1","doi-asserted-by":"publisher","DOI":"10.1016\/0076-6879(90)83036-9"},{"key":"e_1_2_5_74_1","doi-asserted-by":"publisher","DOI":"10.1038\/31927"},{"key":"e_1_2_5_75_1","volume-title":"MEGA: Molecular evolutionary genetic analysis, version 1.0","author":"Kumar S. S.","year":"1993"},{"key":"e_1_2_5_76_1","first-page":"1151","article-title":"Mitochondrial DNA and monocot\u2010dicot divergence time","volume":"12","author":"Laroche J.","year":"1995","journal-title":"Molecular Biology and Evolution"},{"key":"e_1_2_5_77_1","volume-title":"Molecular evolution","author":"Li W.\u2010H.","year":"1997"},{"key":"e_1_2_5_78_1","doi-asserted-by":"publisher","DOI":"10.2307\/2807216"},{"key":"e_1_2_5_79_1","doi-asserted-by":"publisher","DOI":"10.2307\/2666180"},{"key":"e_1_2_5_80_1","doi-asserted-by":"publisher","DOI":"10.1038\/339046a0"},{"key":"e_1_2_5_81_1","first-page":"140","article-title":"Molecular phylogenies in angiosperm evolution","volume":"10","author":"Martin W.","year":"1993","journal-title":"Molecular Biology and Evolution"},{"key":"e_1_2_5_82_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.286.5441.947"},{"key":"e_1_2_5_83_1","doi-asserted-by":"publisher","DOI":"10.2307\/2399900"},{"key":"e_1_2_5_84_1","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/45.4.568"},{"key":"e_1_2_5_85_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-185X.1970.tb01649.x"},{"key":"e_1_2_5_86_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02860537"},{"key":"e_1_2_5_87_1","doi-asserted-by":"publisher","DOI":"10.1080\/106351598261030"},{"key":"e_1_2_5_88_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a026290"},{"key":"e_1_2_5_89_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00178250"},{"key":"e_1_2_5_90_1","doi-asserted-by":"publisher","DOI":"10.1130\/0091-7613(1983)11<503:TDONAG>2.0.CO;2"},{"key":"e_1_2_5_91_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-9822(00)80119-0"},{"key":"e_1_2_5_92_1","doi-asserted-by":"publisher","DOI":"10.2307\/1547810"},{"key":"e_1_2_5_93_1","doi-asserted-by":"publisher","DOI":"10.1038\/29286"},{"key":"e_1_2_5_94_1","doi-asserted-by":"publisher","DOI":"10.1038\/46536"},{"key":"e_1_2_5_95_1","doi-asserted-by":"publisher","DOI":"10.1086\/317584"},{"key":"e_1_2_5_96_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a025940"},{"key":"e_1_2_5_97_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-8137.1972.tb01956.x"},{"key":"e_1_2_5_98_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.255.5052.1697"},{"key":"e_1_2_5_99_1","doi-asserted-by":"publisher","DOI":"10.1016\/0305-1978(92)90067-N"},{"key":"e_1_2_5_100_1","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/46.3.554"},{"key":"e_1_2_5_101_1","doi-asserted-by":"publisher","DOI":"10.2307\/2419767"},{"key":"e_1_2_5_102_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1096-0031.1989.tb00559.x"},{"key":"e_1_2_5_103_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a025731"},{"key":"e_1_2_5_104_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4615-5419-6_9"},{"key":"e_1_2_5_105_1","doi-asserted-by":"publisher","DOI":"10.1002\/j.1537-2197.1996.tb13942.x"},{"key":"e_1_2_5_106_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a026357"},{"key":"e_1_2_5_107_1","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/49.2.306"},{"key":"e_1_2_5_108_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0034-6667(99)00008-1"},{"key":"e_1_2_5_109_1","doi-asserted-by":"publisher","DOI":"10.1080\/106351598261012"},{"key":"e_1_2_5_110_1","doi-asserted-by":"publisher","DOI":"10.2307\/2399952"},{"key":"e_1_2_5_111_1","doi-asserted-by":"publisher","DOI":"10.1038\/46528"},{"key":"e_1_2_5_112_1","doi-asserted-by":"publisher","DOI":"10.2307\/2446539"},{"key":"e_1_2_5_113_1","doi-asserted-by":"publisher","DOI":"10.1002\/j.1537-2197.1993.tb15332.x"},{"key":"e_1_2_5_114_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.282.5394.1692"},{"key":"e_1_2_5_115_1","doi-asserted-by":"publisher","DOI":"10.1038\/21872"},{"key":"e_1_2_5_116_1","volume-title":"PAUP: phylogenetic analysis using parsimony, version 3.0","author":"Swofford D.L.","year":"1991"},{"key":"e_1_2_5_117_1","volume-title":"PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4","author":"Swofford D.L.","year":"2000"},{"key":"e_1_2_5_118_1","first-page":"407","volume-title":"Molecular systematics","author":"Swofford D.L.","year":"1996"},{"key":"e_1_2_5_119_1","first-page":"823","article-title":"Phylogenetic test of the molecular clock and linearized trees","volume":"12","author":"Takezaki N.","year":"1995","journal-title":"Molecular Biology and Evolution"},{"key":"e_1_2_5_120_1","volume-title":"The biology and evolution of fossil plants","author":"Taylor T. N.","year":"1993"},{"key":"e_1_2_5_121_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a025892"},{"key":"e_1_2_5_122_1","first-page":"165","article-title":"Angiospermous pollen (monosulcate\u2010trichotomosulcate phase) from the very early Lower Cretaceous of Southern Tuscany (Italy): some aspects","author":"Trevisan L.","year":"1988","journal-title":"Seventh International Palynological Congress (Brisbane) Abstracts"},{"key":"e_1_2_5_123_1","first-page":"1","article-title":"The megaflora from the Quantico locality (upper Albian), Lower Cretaceous Potomac Group of Virginia","volume":"4","author":"Upchurch G. R.","year":"1994","journal-title":"Virginia Museum of Natural History Memoir"},{"key":"e_1_2_5_124_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.13.7342"},{"key":"e_1_2_5_125_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.86.16.6201"},{"key":"e_1_2_5_126_1","doi-asserted-by":"publisher","DOI":"10.1016\/0169-5347(96)10041-0"},{"key":"e_1_2_5_127_1","first-page":"316","article-title":"Comparison of models for nucleotide substitution used in ML phylogenetic estimates","volume":"11","author":"Yang Z.","year":"1995","journal-title":"Molecular Biology and Evolution"},{"key":"e_1_2_5_128_1","doi-asserted-by":"publisher","DOI":"10.1007\/PL00006320"},{"key":"e_1_2_5_129_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a026389"},{"key":"e_1_2_5_130_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF00160155"}],"container-title":["American Journal of Botany"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.2307%2F3558458","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.2307\/3558458","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.2307\/3558458","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/api.wiley.com\/onlinelibrary\/chorus\/v1\/articles\/10.2307%2F3558458","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/bsapubs.onlinelibrary.wiley.com\/doi\/pdf\/10.2307\/3558458","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T16:23:41Z","timestamp":1759854221000},"score":1,"resource":{"primary":{"URL":"https:\/\/bsapubs.onlinelibrary.wiley.com\/doi\/10.2307\/3558458"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2001,8]]},"references-count":129,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2001,8]]}},"alternative-id":["10.2307\/3558458"],"URL":"https:\/\/doi.org\/10.2307\/3558458","archive":["Portico"],"relation":{},"ISSN":["0002-9122","1537-2197"],"issn-type":[{"value":"0002-9122","type":"print"},{"value":"1537-2197","type":"electronic"}],"subject":[],"published":{"date-parts":[[2001,8]]}}}