Three keys to the radiation of angiosperms into freezing environments

Amy E. Zanne, David C. Tank, William K. Cornwell, Jonathan M. Eastman, Stephen A. Smith, Richard G. Fitzjohn, Daniel J. McGlinn, Brian C. O'Meara, Angela T. Moles, Peter B. Reich, Dana L. Royer, Douglas E. Soltis, Peter F. Stevens, Mark Westoby, Ian J. Wright, Lonnie Aarssen, Robert I. Bertin, Andre Calaminus, Rafaël Govaerts, Frank HemmingsMichelle R. Leishman, Jacek Oleksyn, Pamela S. Soltis, Nathan G. Swenson, Laura Warman, Jeremy M. Beaulieu

Research output: Contribution to journalArticlepeer-review

1110 Scopus citations

Abstract

Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. 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 conduits 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 labile, 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.

Original languageEnglish (US)
Pages (from-to)89-92
Number of pages4
JournalNature
Volume506
Issue number7486
DOIs
StatePublished - 2014

Bibliographical note

Funding Information:
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.

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