Review Article

Palaeobotanical redux: revisiting the age of the angiosperms

  • Nature Plants 3, Article number: 17015 (2017)
  • doi:10.1038/nplants.2017.15
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Abstract

Angiosperms (flowering plants) are the most diverse of all major lineages of land plants and the dominant autotrophs in most terrestrial ecosystems. Their evolutionary and ecological appearance is therefore of considerable interest and has significant implications for understanding patterns of diversification in other lineages, including insects and other animals. More than half a century ago, influential reviews showed that while angiosperms are richly represented in sediments of Late Cretaceous and younger ages, there are no reliable records of angiosperms from pre-Cretaceous rocks. The extensive new macrofossil, mesofossil, and microfossil data that have accumulated since have confirmed and reinforced this pattern. Recently, however, molecular dating methods have raised the possibility that angiosperms may have existed much earlier, and there have been scattered reports of putative angiosperms from Triassic and Jurassic rocks. Critical assessment of these reports shows that, so far, none provide unequivocal evidence of pre-Cretaceous angiosperms. Angiosperms may ultimately be recognized from Jurassic or earlier rocks, but credible palaeobotanical evidence will require unambiguous documentation of the diagnostic structural features that separate angiosperms from other groups of extant and extinct seed plants.

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References

  1. 1.

    , & How old are the angiosperms? Am. J. Sci. 258, 284–299 (1960).

  2. 2.

    Fossil evidence and angiosperm ancestry. Sci. Prog. 49, 84–102 (1961).

  3. 3.

    Palynological evidence on early differentiation of angiosperms. Biol. Rev. 45, 417–450 (1970).

  4. 4.

    & in Origin and Early Evolution of Angiosperms (ed. Beck, C. B.) 139–206 (Columbia University Press, 1976).

  5. 5.

    The Enigma of Angiosperm Origins (Cambridge University Press, 1994).

  6. 6.

    et al. Angiosperm phylogeny: 17 genes, 640 taxa. Am. J. Bot. 98, 704–730 (2011).

  7. 7.

    et al. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402, 404–407 (1999).

  8. 8.

    The Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181, 1–20 (2016).

  9. 9.

    Palaeobiology of Angiosperm Origins (Cambridge University Press, 1976).

  10. 10.

    , & Early Flowers and Angiosperm Evolution (Cambridge University Press, 2011).

  11. 11.

    , & in The Crato Fossil Beds of Brazil: Window into an Ancient World (eds Maill, D. M., Bechly, G. & Loveridge, R. F.) 537–565 (Cambridge University Press, 2007).

  12. 12.

    et al. Archaefructaceae, a new basal angiosperm family. Science 296, 899–904 (2002).

  13. 13.

    & Sinocarpus decussatus gen. et sp. nov., a new angiosperm with syncarpous fruits from the Yixian Formation of Northeast China. Pl. Syst. Evol. 241, 77–88 (2003).

  14. 14.

    , & Kenilanthus, a new eudicot flower with tricolpate pollen from the Early Cretaceous (early-middle Albian) of eastern North America. Grana 56, 161–173, (2016).

  15. 15.

    , , , & Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms. Nature 528, 551–554 (2015).

  16. 16.

    , & Evolution of the angiosperms. Calibrating the tree. Proc. R. Soc. Lond. B 268, 2211–2220 (2001).

  17. 17.

    , & Dating phylogenetically basal eudicots using rbcL sequences and multiple fossil reference points. Am. J. Bot. 92, 1737–1748 (2005).

  18. 18.

    & Angiosperm diversification through time. Am. J. Bot. 96, 349–365 (2009).

  19. 19.

    , & The age and diversification of the angiosperms re-revisited. Am. J. Bot. 97, 1296–1303 (2010).

  20. 20.

    , , & Heterogeneous rates of molecular evolution and diversification could explain the Triassic age estimate for angiosperms. Syst. Biol. 64, 869–878 (2015).

  21. 21.

    , & An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc. Natl Acad. Sci. USA 107, 5897–5902, (2010).

  22. 22.

    Molecular and fossil evidence on the origin of angiosperms. Ann. Rev. Earth Planet. Sci. 40, 301–326 (2012).

  23. 23.

    Recognising angiosperm clades in the Early Cretaceous fossil record. Hist. Biol. 27, 414–429 (2015).

  24. 24.

    et al. Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nat. Commun. 5, 4956 (2014).

  25. 25.

    & Phylogenies and angiosperm diversification. Paleobiology 19, 141–167 (1993).

  26. 26.

    , & The origin and early diversification of angiosperms. Nature 374, 27–33 (1995).

  27. 27.

    , , , & Plant Systematics: a Phylogenetic Approach 2nd edn (Sinauer Associates, 2002).

  28. 28.

    & Defining the limits of flowers: the challenge of distinguishing between the evolutionary products of simple versus compound strobili. Phil. Trans. R. Soc. B 365, 397–409 (2010).

  29. 29.

    , , , & Monetianthus mirus gen. et sp. nov., a nymphaealean flower from the Early Cretaceous of Portugal. Int. J. Plant Sci. 170, 1086–1101 (2009).

  30. 30.

    , , & Canrightiopsis, a new Early Cretaceous fossil with Clavatipollenites-type pollen bridge the gap between extinct Canrightia and extant Chloranthaceae. Grana 54, 184–212 (2015).

  31. 31.

    & Archaeanthus: an early angiosperm from the Cenomanian of the Western Interior of North America. Ann. Missouri Bot. Gard. 71, 351–383 (1984).

  32. 32.

    , , & Lauraceous flowers from the Potomac Group (mid-Cretaceous) of eastern North America. Bot. Gaz. 151, 370–384 (1990).

  33. 33.

    , , & Fossil Kajanthus lusitanicus gen. et sp. nov. from Portugal: floral evidence for Early Cretaceous Lardizabalaceae (Ranunculales, basal eudicot). Grana 53, 283–301 (2014).

  34. 34.

    , , & Archaefructus – angiosperm precursor or specialized early angiosperm? Trends Plant Sci. 8, 369–373 (2003).

  35. 35.

    & Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: ANITA lines and relatives of Chloranthaceae. Int. J. Plant Sci. 175, 555–600 (2014).

  36. 36.

    & Search for antecedents of Early Cretaceous monosulcate columellate pollen. Rev. Palaeobot. Palynol. 83, 175–183 (1994).

  37. 37.

    Plant succession in the English Wealden strata. Proc. Geol. Ass. 86, 439–455 (1975).

  38. 38.

    , & Barremian earliest angiosperm pollen. Palaeontology 22, 513–536 (1979).

  39. 39.

    & Records of angiospermid pollen entry into the English Early Cretaceous succession. Rev. Palaeobot. Palynol. 50, 255–272 (1987).

  40. 40.

    , & Exceptional new record of Cretaceous Hauterivian angiospermid pollen from southern England. J. Micropalaeontol. 10, 75–82 (1991).

  41. 41.

    in Flowering Plant Origin, Evolution and Phylogeny (eds Taylor, D. W. & Hickey, L. J.) 91–115 (Chapman& Hall, 1996).

  42. 42.

    , , & Angiosperm origins. Nature 342, 131 (1989).

  43. 43.

    , , & A review of the angiosperm pollen genus Cretacaeiporites Herngreen, with one new species from the Upper Cretaceous of Egypt. Palynology 41, 101–116 (2015).

  44. 44.

    & Barremian-Aptian angiospermid pollen records from southern England. Rev. Palaeobot. Palynol. 65, 145–151 (1990).

  45. 45.

    & Ultrastructure of Lower Cretaceous angiosperm pollen and the origin and early evolution of flowering plants. Ann. Missouri Bot. Gard. 71, 464–521 (1984).

  46. 46.

    & Angiosperm diversification and Cretaceous floristic trends: a comparison of palynofloras and leaf macrofloras. Paleobiology 16, 77–93 (1990).

  47. 47.

    Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia, U.S.A. Palaeontogr. Abt. B 213, 37–87 (1989).

  48. 48.

    & Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Front. Plant Sci. 4, 344 (2013).

  49. 49.

    & A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). J. Micropalaeontol. 23, 97–104 (2004).

  50. 50.

    & in Pollen and Spores, Patterns of Diversity Systematics Association Special Volume 44 (eds Blackmore, S. & Barnes, S. H.) 169–195 (Clarendon Press, 1991).

  51. 51.

    & Eucommiitheca, a new pollen organ with Eucommiidites pollen from the Early Cretaceous of Portugal. Grana 35, 104–112 (1996).

  52. 52.

    Evidence for a possible gymnospermous affinity for Tricolpites troedssonii Erdtman. New Phytol. 55, 280–285 (1956).

  53. 53.

    On seeds containing Eucommiidites troedssonii pollen from the Jurassic of Grojec, Poland. Bot. J. Linn. Soc. 61, 147–152 (1968).

  54. 54.

    The gymnospermous affinity of Eucommiidites Erdtman, 1948. Rev. Palaeobot. Palynol. 5, 123–127 (1967).

  55. 55.

    , & Pollen organs and seeds with Eucommiidites pollen. Grana 28, 279–294 (1989).

  56. 56.

    , , & Erdtmanitheca portucalensis, a new pollen organ from the Early Cretaceous (Aptian-Albian) of Portugal with Eucommiidites-typepollen. Grana 49, 26–36 (2010).

  57. 57.

    Vladimariales ordo nov. (Gymnospermae) from the Middle Jurassic deposits of the Mikhailovskii Rudnik locality (Kursk Region, European Russia). Paleontol. J. 44, 1281–1307 (2010).

  58. 58.

    et al. Early Cretaceous Umkomasia from Mongolia: implications for homology of corystosperm cupules. New Phytol. 210, 1418–1429 (2016).

  59. 59.

    & Caytonanthus pollen from the Lower and Middle Jurassic. GeoSkrifter 24, 255–267 (1986).

  60. 60.

    , & Angiosperm floral structures from the Early Cretaceous of Portugal. Plant Syst. Evol. 8, 31–49 (1994).

  61. 61.

    , & New diversity among Chlamydospermous seeds from the Early Cretaceous of Portugal and North America. Int. J. Plant Sci. 174, 530–558 (2013).

  62. 62.

    et al. Phase contrast enhanced synchrotron-radiation X-ray analyses of Cretaceous seeds link Gnetales to extinct Bennettitales. Nature 450, 549–552 (2007).

  63. 63.

    , & Early Cretaceous mesofossils from Portugal and eastern North America related to the Bennettitales-Erdtmanithecales-Gnetales group. Am. J. Bot. 96, 252–283 (2009).

  64. 64.

    , & Welwitschioid diversity in the Early Cretaceous: evidence from fossil seeds with pollen from Portugal and eastern North America. Grana 53, 175–196 (2014).

  65. 65.

    A plant with flower-like organs from the Wealden of the Weald (Lower Cretaceous), southern England. Cretaceous Res. 17, 27–38 (1996).

  66. 66.

    , , , & Montsechia, an ancient aquatic angiosperm. Proc. Natl Acad. Sci. USA 112, 10985–10988 (2015).

  67. 67.

    & The earliest ascidiate carpel and its implications for angiosperm evolution. Acta Geol. Sinica 85, 998–1112 (2011).

  68. 68.

    Early Cretaceous sarraceniacean-like pitcher plants from China. Acta Bot. Gallica 152, 227–234 (2005).

  69. 69.

    , , , & Early Cretaceous Archaeamphora is not a carnivorous angiosperm. Front. Plant Sci. (2015).

  70. 70.

    , , & A new angiosperm genus from the Lower Cretaceous Yixian Formation, western Liaoning, China. Acta Geol. Sinica 87, 916–925, (2013).

  71. 71.

    & The earliest normal flower from Liaoning Province, China. J. Integr. Plant Biol. 51, 800–811 (2009).

  72. 72.

    The oldest angiosperm – a tricarpous female reproductive fossil from western Liaoning Province, NE China. Sci. China Ser. D-Earth Sci. 41, 14–20 (1998).

  73. 73.

    A systematic classification of Ephedraceae: living and fossil. Phytotaxa 158, 283–290 (2014).

  74. 74.

    & Macrofossil evidence unveiling evolution and ecology of early Ephedraceae. Perspect. Plant Ecol. Evol. Syst. 17, 331–346 (2015).

  75. 75.

    Early Cretaceous flora of Mongolia. Palaeontogr. Abt. B 181, 1–43 (1982).

  76. 76.

    , , & In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science 282, 1692–1695 (1998).

  77. 77.

    , The leaf venation and reproductive structures of a Late Triassic angiosperm, Sanmiguelia lewisii. Taxon 36, 778–779 (1987).

  78. 78.

    & A perfect flower from the Jurassic of China. Hist. Biol. 28, 707–719 (2015).

  79. 79.

    et al. A whole plant herbaceous angiosperm from the Middle Jurassic of China. Acta Geol. Sinica 90, 19–29 (2016).

  80. 80.

    & Yuhania : a unique angiosperm from the Middle Jurassic of Inner Mongolia, China. Hist. Biol. (2016).

  81. 81.

    & Xingxueanthus: an enigmatic Jurassic seed plant and its implications for the origin of angiospermy. Acta Geol. Sinica 84, 47–55 (2010).

  82. 82.

    , , , & Schmeissneria: a missing link to angiosperms? BMC Evol. Biol. 7, 14 (2007).

  83. 83.

    Schmeissneria: an angiosperm from the Early Jurassic. J. Syst. Evol. 48, 326–335 (2010).

  84. 84.

    The Early Jurassic male ginkgoalean inflorescence Stachyopitys preslii Schenk and its in situ pollen. Scr. Geol. Special Issue 7, 141–149 (2010).

  85. 85.

    & An undercover angiosperm from the Jurassic of China. Acta Geol. Sinica 84, 895–902 (2010).

  86. 86.

    , , & Pollen cones and associated leaves from the Lower Cretaceous of China and a re-evaluation of Mesozoic male cycad cones. J. Syst. Palaeontol. 12, 1001–1023 (2014).

  87. 87.

    & Gnetalean plants from the Jurassic of Ust–Balej, East Siberia. Rev. Palaeobot. Palynol. 53, 359–374 (1988).

  88. 88.

    & An angiosperm cradle community and new proangiosperm taxa. Acta Palaeobot. Suppl. 2, 111–127 (1999).

  89. 89.

    & Comparative pollen morphology and ultrastructure of modern and fossil gnetophytes. Rev. Palaeobot. Palynol. 156, 130–138 (2009).

  90. 90.

    & Bernardes- Endressinia brasiliana, a Magnolialean Angiosperm from the Lower Cretaceous Crato Formation (Brazil). Int. J. Plant Sci. 165, 1121–1133 (2004).

  91. 91.

    , & Pluricarpellatia, a nymphaealean angiosperm from the Lower Cretaceous of northern Gondwana (Crato Formation, Brazil). Taxon 57, 1147–1158 (2008).

  92. 92.

    & Taxonomy and palaeoecology of Early Cretaceous (Late Albian) angiosperm leaves from Alexander Island, Antarctica. Rev. Palaeobot. Palynol. 92, 1–28 (1996).

  93. 93.

    Cuticle evolution in Early Cretaceous angiosperms from the Potomac Group of Virginia and Maryland. Ann. Missouri Bot. Gard. 71, 522–550 (1984).

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Acknowledgements

We thank the Institute of Vertebrate Paleontology and Paleoanthropology in Beijing, China for loaning the specimen of Solaranthus daohugensis and C. Pott for photographing this specimen and the Tsuga cone. We thank P. von Knorring for creating Figs 1 and 2. We thank J. Doyle and two anonymous reviewers for constructive comments on the manuscript. This work was funded in part by NSF grant DEB-1348456 to P.S.H. and P.R.C. and the Swedish Research Council grant 2014-5228 to E.M.F.

Author information

Affiliations

  1. Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60022, USA.

    • Patrick S. Herendeen
  2. Department of Palaeobiology, Swedish Museum of Natural History, SE-104 05 Stockholm, Sweden.

    • Else Marie Friis
  3. Department of Earth Science, University of Aarhus, DK-8000 Aarhus, Denmark.

    • Kaj Raunsgaard Pedersen
  4. Oak Spring Garden Foundation, 1776 Loughborough Lane, Upperville, Virginia 20184, USA.

    • Peter R. Crane
  5. Yale School of Forestry and Environmental Studies, 195 Prospect Street, New Haven, Connecticut 06511, USA.

    • Peter R. Crane

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Contributions

All authors contributed to the design and scope of the paper, and evaluations of the fossil taxa discussed in the paper. All authors contributed to writing and revising the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Patrick S. Herendeen.