Three keys to the radiation of angiosperms into freezing environments

Journal name:
Nature
Volume:
506,
Pages:
89–92
Date published:
DOI:
doi:10.1038/nature12872
Received
Accepted
Published online
Corrected online

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.

At a glance

Figures

  1. Time-calibrated maximum-likelihood estimate of the molecular phylogeny for 31,749 species of seed plants.
    Figure 1: Time-calibrated maximum-likelihood estimate of the molecular phylogeny for 31,749 species of seed plants.

    The four major angiosperm lineages discussed in the text are highlighted: Monocotyledoneae (green), Magnoliidae (blue), Superrosidae (brown) and Superasteridae (yellow). Non-seed plant outgroups (that is, bryophytes, lycophytes and monilophytes) were removed for the purposes of visualization.

  2. Coordinated evolutionary transition rates between leaf phenology or conduit diameter and climate occupancy.
    Figure 2: Coordinated evolutionary transition rates between leaf phenology or conduit diameter and climate occupancy.

    a, b, A representation of coordinated evolution for the best likelihood-based model between leaf phenology for 2,630 species (evergreen,dark green; deciduous,light green) and climate occupancy (freezing exposed (freezing), striped; freezing unexposed (not freezing),solid) (a), and conduit diameter for 860 species (large (≥0.044mm),light blue; small (<0.044mm),dark blue) and climate occupancy (b) based on models fit to all Angiospermae. The sizes of the black arrows in the plot are proportional to the transition rates between each possible state combination (larger arrows denote higher rates; no arrows for rates of 0). The number at the top of each panel denotes the number of extant Angiospermae species used in the analyses and percentages denote the percentage of extant species with that character state. The size of each circle is proportional to the persistence time in that state, where persistence time is defined as the inverse of the sum of the transition rates away from a given character state (that is, the inverse of the sum of all arrow rates out of a character state). c, d, The relative likelihood of the different pathways out of the evergreen and freezing-unexposed state and into the deciduous and freezing-exposed state (c), and out of the large-diameter conduit and freezing-unexposed state and into the small-diameter conduit and freezing-exposed state (d). The three possible pathways between two focal character state combinations provide insight into whether lineages typically evolved: (1) with the trait first, such that phenology or conduit diameter shifted before encountering freezing; (2) with climate occupancy first, such that phenology or conduit diameter shifted after encountering freezing; or (3) both simultaneously, such that shifts in phenology or conduit diameter and encountering freezing happened at the same time (see Supplementary Information for further details).

  3. Coordinated evolutionary transition rates between growth form and climate occupancy.
    Figure 3: Coordinated evolutionary transition rates between growth form and climate occupancy.

    a, A representation of coordinated evolution for the best likelihood-based model between growth form for 12,706 species (herbaceous, green; woody,brown) and climate occupancy based on a model assuming the same rates were applied to all Angiospermae (top plot above the dashed arrow), and the best-fit model, in which rates were estimated separately for the major lineages, that is, Monocotyledoneae, Magnoliidae, Superrosidae and Superasteridae (bottom four plots below the dashed arrows). b, The weighted average (by clade diversity) of the relative likelihood of the different pathways out of the woody and freezing-unexposed state and into the herbaceous and freezing-exposed state (see Fig. 2 and Methods for further details).

  4. Examples of the definition of /`woody/'.
    Extended Data Fig. 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.).

  5. Reference timetree used for congruification analyses.
    Extended Data Fig. 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.

Tables

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

Change history

Corrected online 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, 289306 (1915)
  2. Wing, S. L. & Boucher, L. D. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26, 379421 (1998)
  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, 82107 (2004)
  4. Moles, A. T. et al. Global patterns in plant height. J. Ecol. 97, 923932 (2009)
  5. Tyree, M. T. & Zimmermann, M. H. Xylem Structure and the Ascent of Sap (Springer, 2002)
  6. Cronquist, A. The Evolution and Classification of Flowering Plants. (Houghton Mifflin, 1968)
  7. Kattge, J. et al. TRY—a global database of plant traits. Glob. Change Biol. 17, 29052935 (2011)
  8. Stebbins, G. L. The probable growth habit of the earliest flowering plants. Ann. Mo. Bot. Gard. 52, 457468 (1965)
  9. Taylor, D. & Hickey, L. Phylogenetic evidence for the herbaceous origin of angiosperms. Plant Syst. Evol. 180, 137156 (1992)
  10. Soltis, D. E. et al. Angiosperm phylogeny: 17 genes, 640 taxa. Am. J. Bot. 98, 704730 (2011)
  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, 58975902 (2010)
  12. Spicer, R. & Groover, A. Evolution of development of vascular cambia and secondary growth. New Phytol. 186, 577592 (2010)
  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, 596609 (2012)
  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, 142152 (2008)
  15. Wiens, J. J. & Donoghue, M. J. Historical biogeography, ecology and species richness. Trends Ecol. Evol. 19, 639644 (2004)
  16. Donoghue, M. J. A phylogenetic perspective on the distribution of plant diversity. Proc. Natl Acad. Sci. USA 105, 1154911555 (2008)
  17. Wheeler, E. A., Baas, P. & Rodgers, S. Variations in dicot wood anatomy: a global analysis based on the Insidewood database. IAWA J. 28, 229258 (2007)
  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, 709725 (2000)
  19. Judd, W. S., Sanders, R. W. & Donoghue, M. J. Angiosperm family pairs: preliminary phylogenetic analysis. Harv. Pap. Bot. 5, 149 (1994)
  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, 602611 (2008)
  21. Loehle, C. Height growth rate tradeoffs determine northern and southern range limits for trees. J. Biogeogr. 25, 735742 (1998)
  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, 13671372 (1999)
  23. Maddison, W. P. Confounding asymmetries in evolutionary diversification and character change. Evolution 60, 17431746 (2006)
  24. Soltis, D. E. et al. Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach. Am. J. Bot. 100, 916929 (2013)
  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, 12991307 (2011)
  26. Groover, A. T. What genes make a tree a tree? Trends Plant Sci. 10, 210214 (2005)
  27. Lens, F., Smets, E. & Melzer, S. Stem anatomy supports Arabidopsis thaliana as a model for insular woodiness. New Phytol. 193, 1217 (2012)
  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, 17411755 (2013)
  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, 725737 (2013)

Download references

Author information

Affiliations

  1. Department of Biological Sciences, George Washington University, Washington DC 20052, USA

    • Amy E. Zanne
  2. Center for Conservation and Sustainable Development, Missouri Botanical Garden, St Louis, Missouri 63121, USA

    • Amy E. Zanne
  3. Department of Biological Sciences, University of Idaho, Moscow, Idaho 83844, USA

    • David C. Tank &
    • Jonathan M. Eastman
  4. Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, Idaho 83844, USA

    • David C. Tank &
    • Jonathan M. Eastman
  5. Department of Ecological Sciences, Systems Ecology, de Boelelaan 1085, 1081 HV Amsterdam, the Netherlands

    • William K. Cornwell
  6. Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia

    • William K. Cornwell,
    • Angela T. Moles,
    • Frank Hemmings &
    • Laura Warman
  7. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Stephen A. Smith
  8. Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia V6T1Z4, Canada

    • Richard G. FitzJohn
  9. Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia

    • Richard G. FitzJohn,
    • Mark Westoby,
    • Ian J. Wright &
    • Michelle R. Leishman
  10. Department of Biology and the Ecology Center, Utah State University, Logan, Utah 84322, USA

    • Daniel J. McGlinn
  11. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996, USA

    • Brian C. O’Meara
  12. Department of Forest Resources, University of Minnesota, St Paul, Minnesota 55108, USA

    • Peter B. Reich &
    • Jacek Oleksyn
  13. Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, New South Wales 2751, Australia

    • Peter B. Reich
  14. Department of Earth and Environmental Sciences, Wesleyan University, Middletown, Connecticut 06459, USA

    • Dana L. Royer
  15. Department of Biology, University of Florida, Gainesville, Florida 32611, USA

    • Douglas E. Soltis &
    • Andre Calaminus
  16. Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA

    • Douglas E. Soltis &
    • Pamela S. Soltis
  17. Genetics Institute, University of Florida, Gainesville, Florida 32611, USA

    • Douglas E. Soltis &
    • Pamela S. Soltis
  18. Department of Biology, University of Missouri—St Louis, St Louis, Missouri 63121, USA

    • Peter F. Stevens
  19. Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada

    • Lonnie Aarssen
  20. Department of Biology, College of the Holy Cross, Worcester, Massachusetts 01610, USA

    • Robert I. Bertin
  21. Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, United Kingdom

    • Rafaël Govaerts
  22. Polish Academy of Sciences, Institute of Dendrology, 62-035 Kornik, Poland

    • Jacek Oleksyn
  23. Department of Plant Biology and Ecology, Evolutionary Biology and Behavior, Program, Michigan State University, East Lansing, Michigan 48824, USA

    • Nathan G. Swenson
  24. Institute of Pacific Islands Forestry, USDA Forest Service, Hilo, Hawaii 96720, USA

    • Laura Warman
  25. National Institute for Mathematical & Biological Synthesis, University of Tennessee, Knoxville, Tennessee 37996, USA

    • Jeremy M. Beaulieu

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

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/).

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Examples of the definition of ‘woody’. (1,581 KB)

    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.).

  2. Extended Data Figure 2: Reference timetree used for congruification analyses. (455 KB)

    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 Tables

  1. Extended Data Table 1: Number of species in different growth forms by clade (538 KB)
  2. Extended Data Table 2: Coordinated evolutionary model fits for leaf phenology, conduit diameter and climate occupancy (78 KB)
  3. Extended Data Table 3: Coordinated evolutionary model transition rates (393 KB)
  4. Extended Data Table 4: Coordinated evolutionary model fits for growth form and climate occupancy (54 KB)

Supplementary information

PDF files

  1. Supplementary Information (2.8 MB)

    This file contains Supplementary Methods, Supplementary References and Supplementary Tables 1-4.

Additional data