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Link to original content: http://dx.doi.org/10.1038/nature02361
Ferns diversified in the shadow of angiosperms | Nature
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Ferns diversified in the shadow of angiosperms

Nature volume 428, pages 553–557 (2004)Cite this article

Abstract

The rise of angiosperms during the Cretaceous period is often portrayed as coincident with a dramatic drop in the diversity and abundance of many seed-free vascular plant lineages, including ferns1,2,3,4,5. This has led to the widespread belief that ferns, once a principal component of terrestrial ecosystems6, succumbed to the ecological predominance of angiosperms and are mostly evolutionary holdovers from the late Palaeozoic/early Mesozoic era. The first appearance of many modern fern genera in the early Tertiary fossil record implies another evolutionary scenario; that is, that the majority of living ferns resulted from a more recent diversification7,8,9,10. But a full understanding of trends in fern diversification and evolution using only palaeobotanical evidence is hindered by the poor taxonomic resolution of the fern fossil record in the Cretaceous11. Here we report divergence time estimates for ferns and angiosperms based on molecular data, with constraints from a reassessment of the fossil record. We show that polypod ferns (> 80% of living fern species) diversified in the Cretaceous, after angiosperms, suggesting perhaps an ecological opportunistic response to the diversification of angiosperms, as angiosperms came to dominate terrestrial ecosystems.

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Figure 1: Phylogenetic chronograms of ferns (a) and angiosperms (b), and proportional lineages-through-time (LTT) plots for angiosperms and polypods (c).

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References

  1. Crane, P. R. in The Origin of Angiosperms and Their Biological Consequences (eds Friis, E. M., Chaloner, W. G. & Crane, P. R.) 107–144 (Cambridge Univ. Press, Cambridge, 1987)

    Google Scholar 

  2. Lidgard, S. & Crane, P. R. Angiosperm diversification and Cretaceous floristic trends: A comparison of palynofloras and leaf macrofloras. Paleobiology 16, 77–93 (1990)

    Article  Google Scholar 

  3. Crane, P. R., Friis, E. M. & Pedersen, K. R. The origin and early diversification of angiosperms. Nature 374, 27–33 (1995)

    Article  ADS  CAS  Google Scholar 

  4. Lupia, R., Lidgard, S. & Crane, P. R. Comparing palynological abundance and diversity: Implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology 25, 305–340 (1999)

    Article  Google Scholar 

  5. Nagalingum, N. S., Drinnan, A. N., Lupia, R. & McLoughlin, S. Fern spore diversity and abundance in Australia during the Cretaceous. Rev. Palaeobot. Palynol. 119, 69–92 (2002)

    Article  Google Scholar 

  6. Niklas, K. J., Tiffney, B. H. & Knoll, A. H. Patterns in vascular land plant diversification. Nature 303, 614–616 (1983)

    Article  ADS  Google Scholar 

  7. Smith, A. R. Comparison of fern and flowering plant distributions with some evolutionary interpretations for ferns. Biotropica 4, 4–9 (1972)

    Article  Google Scholar 

  8. Lovis, J. D. Evolutionary patterns and processes in ferns. Adv. Bot. Res. 4, 229–415 (1977)

    Article  Google Scholar 

  9. Rothwell, G. W. in Pteridology in Perspective (eds Camus, J. M., Gibby, M. & Johns, R. J.) 395–404 (Royal Botanic Gardens, Kew, 1996)

    Google Scholar 

  10. Collinson, M. E. in Pteridology in Perspective (eds Camus, J. M., Gibby, M. & Johns, R. J.) 349–394 (Royal Botanic Gardens, Kew, 1996)

    Google Scholar 

  11. Schneider, H. & Kenrick, P. An Early Cretaceous root-climbing epiphyte (Lindsaeaceae) and its significance for calibrating the diversification of polypodiaceous ferns. Rev. Palaeobot. Palynol. 115, 33–41 (2001)

    Article  CAS  PubMed  Google Scholar 

  12. Dilcher, D. L. Paleobotany: Some aspects of non-flowering and flowering plant evolution. Taxon 50, 697–711 (2001)

    Article  Google Scholar 

  13. Friis, E. M., Pederson, K. R. & Crane, P. R. Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous. Nature 410, 357–360 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Soltis, D. E. et al. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. J. Linn. Soc. Bot. 133, 381–461 (2000)

    Article  Google Scholar 

  15. Soltis, P. S., Soltis, D. E. & Chase, M. W. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402–404 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Qiu, Y.-L. et al. The earliest angiosperms: Evidence from mitochondrial, plastid and nuclear genomes. Nature 402, 404–407 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Skog, J. E. Biogeography of Mesozoic leptosporangiate ferns related to extant ferns. Brittonia 53, 236–269 (2001)

    Article  Google Scholar 

  18. Pryer, K. M. et al. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409, 618–622 (2001)

    Article  CAS  PubMed  Google Scholar 

  19. Deng, S. Ecology of the Early Cretaceous ferns of Northeast China. Rev. Palaeobot. Palynol. 119, 93–112 (2002)

    Article  Google Scholar 

  20. Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Mol. Biol. Evol. 19, 101–109 (2002)

    Article  CAS  PubMed  Google Scholar 

  21. Pagel, M. & Lutzoni, F. in Biological Evolution and Statistical Physics (eds Lässig, M. & Valleriani, A.) 148–161 (Springer, Berlin, 2002)

    Book  Google Scholar 

  22. Magallón, S. & Sanderson, M. J. Absolute diversification rates in angiosperm clades. Evolution 55, 1762–1780 (2001)

    PubMed  Google Scholar 

  23. Wikström, N., Savolainen, V. & Chase, M. W. Evolution of the angiosperms: Calibrating the family tree. Proc. R. Soc. Lond. B 268, 2211–2220 (2001)

    Article  Google Scholar 

  24. Benton, M. J. & Ayala, F. J. Dating the Tree of Life. Science 300, 1698–1700 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Soltis, P. S., Soltis, D. E., Savolainen, V., Crane, P. R. & Barraclough, T. G. Rate heterogeneity among lineages of tracheophytes: Integration of molecular and fossil data and evidence for molecular living fossils. Proc. Natl Acad. Sci. USA 99, 4430–4435 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wikström, N. & Kenrick, P. Evolution of Lycopodiaceae (Lycopsida): Estimating divergence times from rbcL gene sequences by use of nonparametric rate smoothing. Mol. Phylogenet. Evol. 19, 177–186 (2001)

    Article  PubMed  Google Scholar 

  27. Kawai, H. et al. Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421, 287–290 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Smith, H. Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407, 585–591 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  29. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    Article  CAS  PubMed  Google Scholar 

  30. Sanderson, M. J. r8s: Inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302 (2003)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Duke Biology systematics discussion group, especially P. Manos, for suggestions; F. Lutzoni, N. Nagalingum and A. R. Smith for comments on the manuscript; and M. Skakuj for the thumbnail sketches included in Fig. 1. This work was supported in part by grants from the National Science Foundation to H.S., K.M.P., R.C. and R.L.; by the Deep Time Research Coordination Network (NSF); and by the A.W. Mellon Foundation Fund to Duke University for Plant Systematics.

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Authors and Affiliations

  1. Department of Biology, Duke University, Durham, North Carolina, 27708, USA

    Harald Schneider, Eric Schuettpelz & Kathleen M. Pryer

  2. Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Abteilung Systematische Botanik, Georg-August-Universität, Untere Karspüle 2, 37073, Göttingen, Germany

    Harald Schneider

  3. University Herbarium, University of California, 1001 Valley Life Sciences Building #2465, Berkeley, California, 94720, USA

    Raymond Cranfill

  4. Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México, Circuito Exterior, Anexo al Jardín Botánico, AP 70-233, DF 04510, México, Mexico

    Susana Magallón

  5. Sam Noble Oklahoma Museum of Natural History, University of Oklahoma, Norman, Oklahoma, 73072, USA

    Richard Lupia

  6. School of Geology and Geophysics, University of Oklahoma, Norman, Oklahoma, 73072, USA

    Richard Lupia

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  1. Harald Schneider
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Correspondence to Kathleen M. Pryer.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Information

Provides our re-evaluation of the fossil record of major fern lineages and a synopsis of fossil fern constraints applied in this study (DOC 85 kb)

Supplementary Table 1

Provides rbcL and rps4 vouchers/citations and GenBank accession numbers for taxa not in Soltis et al. 2000. (XLS 51 kb)

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Schneider, H., Schuettpelz, E., Pryer, K. et al. Ferns diversified in the shadow of angiosperms. Nature 428, 553–557 (2004). https://doi.org/10.1038/nature02361

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