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Three keys to the radiation of angiosperms into freezing environments

A Corrigendum to this article was published on 20 May 2015

A Corrigendum to this article was published on 15 October 2014

This article has been updated

Abstract

Early flowering plants are thought to have been woody species restricted to warm habitats1,2,3. This lineage has since radiated into almost every climate, with manifold growth forms4. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species’ traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits5 and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile6, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.

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Figure 1: Time-calibrated maximum-likelihood estimate of the molecular phylogeny for 31,749 species of seed plants.
Figure 2: Coordinated evolutionary transition rates between leaf phenology or conduit diameter and climate occupancy.
Figure 3: Coordinated evolutionary transition rates between growth form and climate occupancy.

Change history

  • 03 January 2014

    The Dryad Digital Repository doi number has been updated.

References

  1. Sinnott, E. W. & Bailey, I. W. The evolution of herbaceous plants and its bearing on certain problems of geology and climatology. J. Geol. 23, 289–306 (1915)

    Article  ADS  Google Scholar 

  2. Wing, S. L. & Boucher, L. D. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26, 379–421 (1998)

    Article  CAS  ADS  Google Scholar 

  3. Feild, T. S., Arens, N. C., Doyle, J. A., Dawson, T. E. & Donoghue, M. J. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30, 82–107 (2004)

    Article  Google Scholar 

  4. Moles, A. T. et al. Global patterns in plant height. J. Ecol. 97, 923–932 (2009)

    Article  Google Scholar 

  5. Tyree, M. T. & Zimmermann, M. H. Xylem Structure and the Ascent of Sap (Springer, 2002)

    Book  Google Scholar 

  6. Cronquist, A. The Evolution and Classification of Flowering Plants. (Houghton Mifflin, 1968)

    Google Scholar 

  7. Kattge, J. et al. TRY—a global database of plant traits. Glob. Change Biol. 17, 2905–2935 (2011)

    Article  ADS  Google Scholar 

  8. Stebbins, G. L. The probable growth habit of the earliest flowering plants. Ann. Mo. Bot. Gard. 52, 457–468 (1965)

    Article  Google Scholar 

  9. Taylor, D. & Hickey, L. Phylogenetic evidence for the herbaceous origin of angiosperms. Plant Syst. Evol. 180, 137–156 (1992)

    Article  Google Scholar 

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

    Article  Google Scholar 

  11. Smith, S. A., Beaulieu, J. M. & Donoghue, M. J. An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc. Natl Acad. Sci. USA 107, 5897–5902 (2010)

    Article  CAS  ADS  Google Scholar 

  12. Spicer, R. & Groover, A. Evolution of development of vascular cambia and secondary growth. New Phytol. 186, 577–592 (2010)

    Article  CAS  Google Scholar 

  13. Feild, T. S. & Wilson, J. P. Evolutionary voyage of angiosperm vessel structure-function and its significance for early angiosperm success. Int. J. Plant Sci. 173, 596–609 (2012)

    Article  Google Scholar 

  14. Philippe, M. et al. Woody or not woody? Evidence for early angiosperm habit from the Early Cretaceous fossil wood record of Europe. Palaeoworld 17, 142–152 (2008)

    Article  Google Scholar 

  15. Wiens, J. J. & Donoghue, M. J. Historical biogeography, ecology and species richness. Trends Ecol. Evol. 19, 639–644 (2004)

    Article  Google Scholar 

  16. Donoghue, M. J. A phylogenetic perspective on the distribution of plant diversity. Proc. Natl Acad. Sci. USA 105, 11549–11555 (2008)

    Article  CAS  ADS  Google Scholar 

  17. Wheeler, E. A., Baas, P. & Rodgers, S. Variations in dicot wood anatomy: a global analysis based on the Insidewood database. IAWA J. 28, 229–258 (2007)

    Article  Google Scholar 

  18. Botta, A., Viovy, N., Ciais, P., Friedlingstein, P. & Monfray, P. A global prognostic scheme of leaf onset using satellite data. Glob. Change Biol. 6, 709–725 (2000)

    Article  ADS  Google Scholar 

  19. Judd, W. S., Sanders, R. W. & Donoghue, M. J. Angiosperm family pairs: preliminary phylogenetic analysis. Harv. Pap. Bot. 5, 1–49 (1994)

    Google Scholar 

  20. Paton, A. J. et al. Towards target 1 of the global strategy for plant conservation: a working list of all known plant speciesprogress and prospects. Taxon 57, 602–611 (2008)

    Google Scholar 

  21. Loehle, C. Height growth rate tradeoffs determine northern and southern range limits for trees. J. Biogeogr. 25, 735–742 (1998)

    Article  Google Scholar 

  22. Davis, S. D., Sperry, J. S. & Hacke, U. G. The relationship between xylem conduit diameter and cavitation caused by freezing. Am. J. Bot. 86, 1367–1372 (1999)

    Article  CAS  Google Scholar 

  23. Maddison, W. P. Confounding asymmetries in evolutionary diversification and character change. Evolution 60, 1743–1746 (2006)

    Article  Google Scholar 

  24. Soltis, D. E. et al. Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach. Am. J. Bot. 100, 916–929 (2013)

    Article  Google Scholar 

  25. Thomson, F. J., Moles, A. T., Auld, T. D. & Kingsford, R. T. Seed dispersal distance is more strongly correlated with plant height than with seed mass. J. Ecol. 99, 1299–1307 (2011)

    Article  Google Scholar 

  26. Groover, A. T. What genes make a tree a tree? Trends Plant Sci. 10, 210–214 (2005)

    Article  CAS  Google Scholar 

  27. Lens, F., Smets, E. & Melzer, S. Stem anatomy supports Arabidopsis thaliana as a model for insular woodiness. New Phytol. 193, 12–17 (2012)

    Article  Google Scholar 

  28. Jansson, R., Rodríguez-Castañeda, G. & Harding, L. E. What can multiple phylogenies say about the latitudinal diversity gradient? A new look at the tropical conservatism, out-of-the-tropics and diversification rate hypotheses. Evolution 67, 1741–1755 (2013)

    Article  Google Scholar 

  29. Beaulieu, J. M., O’Meara, B. C. & Donoghue, M. J. Identifying hidden rate changes in the evolution of a binary morphological character: the evolution of plant habit in campanulid angiosperms. Syst. Biol. 62, 725–737 (2013)

    Article  Google Scholar 

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Acknowledgements

We thank T. Robertson and A. Hahn at the Global Biodiversity Information Facility for providing species’ georeference points, A. Ordonez for providing growth form data, and A. Miller and D. Ackerly for helpful comments on a draft of this manuscript. Support for this work was given to the working group “Tempo and Mode of Plant Trait Evolution: Synthesizing Data from Extant and Extinct Taxa” by the National Evolutionary Synthesis Center (NESCent), National Science Foundation grant #EF- 0905606 and Macquarie University Genes to Geoscience Research Centre.

Author information

Authors and Affiliations

Authors

Contributions

A.E.Z., W.K.C., D.C.T. and J.M.B. designed the initial project, wrote the original manuscript and carried out analyses. J.M.E., S.A.S. and D.C.T. constructed the timetree. J.M.E., R.G.F., D.J.M., B.C.O’M. and S.A.S. were major quantitative contributors, especially with the development of new methods, analyses, graphics and writing. A.T.M., P.B.R., D.L.R., D.E.S., P.F.S., I.J.W. and M.W. were large contributors through the development of initial ideas, methods, dataset curation, analyses and writing. L.A., R.I.B., A.C., R.G., F.H., M.R.L., J.O., P.S.S., N.G.S. and L.W. contributed data sets and discussions, and read drafts.

Corresponding author

Correspondence to Amy E. Zanne.

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Competing interests

The authors declare no competing financial interests.

Additional information

Data and code are deposited at the Dryad Digital Repository (http://dx.doi.org/10.5061/dryad.63q27) and TRY (http://www.try-db.org/).

Extended data figures and tables

Extended Data Figure 1 Examples of the definition of ‘woody’.

ad, We defined ‘woody’ as having a prominent aboveground stem that is persistent over time and with changing environmental conditions. a, Liriodendron tulipifera (Magnoliaceae), Joyce Kilmer Memorial Forest, Robbinsville, North Carolina, USA. b, Carnegiea giganteana (Cactaceae), Biosphere II, Tucson, Arizona, USA, c, Rhopalostylis sapida (Arecaceae) and Cyathea sp. (Cyatheaceae), Punakaiki, South Island, New Zealand. d, Pandanus sp. (Pandanaceae), Moreton Bay Research Station, North Stradbroke Island, Queensland, Australia (photographs by A.E.Z.).

Extended Data Figure 2 Reference timetree used for congruification analyses.

Results of the divergence time estimation of 639 taxa of seed plants from the reanalysis of a previously described10 phylogeny. Fossil calibrations are indicated at the nodes with green circles, and numbers correspond to fossils described in Supplementary Table 2. Concentric dashed circles represent 100-Myr intervals as indicated by the scale bar.

Extended Data Table 1 Number of species in different growth forms by clade
Extended Data Table 2 Coordinated evolutionary model fits for leaf phenology, conduit diameter and climate occupancy
Extended Data Table 3 Coordinated evolutionary model transition rates
Extended Data Table 4 Coordinated evolutionary model fits for growth form and climate occupancy

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary References and Supplementary Tables 1-4. (PDF 2886 kb)

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Zanne, A., Tank, D., Cornwell, W. et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92 (2014). https://doi.org/10.1038/nature12872

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