title: Three keys to the radiation of angiosperms into freezing environments.
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.
authors.affiliation: 1] Department of Biological Sciences, George Washington University, Washington DC 20052, USA [2] Center for Conservation and Sustainable Development, Missouri Botanical Garden, St Louis, Missouri 63121, USA.
authors.forename: Amy E
authors.initials: AE
authors.lastname: Zanne
authors.affiliation: 1] Department of Biological Sciences, University of Idaho, Moscow, Idaho 83844, USA [2] Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, Idaho 83844, USA.
authors.forename: David C
authors.initials: DC
authors.lastname: Tank
authors.affiliation: 1] Department of Ecological Sciences, Systems Ecology, de Boelelaan 1085, 1081 HV Amsterdam, the Netherlands [2] Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia.
authors.forename: William K
authors.initials: WK
authors.lastname: Cornwell
authors.affiliation: 1] Department of Biological Sciences, University of Idaho, Moscow, Idaho 83844, USA [2] Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, Idaho 83844, USA.
authors.forename: Jonathan M
authors.initials: JM
authors.lastname: Eastman
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA.
authors.forename: Stephen A
authors.initials: SA
authors.lastname: Smith
authors.affiliation: 1] Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia V6T1Z4, Canada [2] Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia.
authors.forename: Richard G
authors.initials: RG
authors.lastname: FitzJohn
authors.affiliation: Department of Biology and the Ecology Center, Utah State University, Logan, Utah 84322, USA.
authors.forename: Daniel J
authors.initials: DJ
authors.lastname: McGlinn
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996, USA.
authors.forename: Brian C
authors.initials: BC
authors.lastname: O'Meara
authors.affiliation: Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia.
authors.forename: Angela T
authors.initials: AT
authors.lastname: Moles
authors.affiliation: 1] Department of Forest Resources, University of Minnesota, St Paul, Minnesota 55108, USA [2] Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, New South Wales 2751, Australia.
authors.forename: Peter B
authors.initials: PB
authors.lastname: Reich
authors.affiliation: Department of Earth and Environmental Sciences, Wesleyan University, Middletown, Connecticut 06459, USA.
authors.forename: Dana L
authors.initials: DL
authors.lastname: Royer
authors.affiliation: 1] Department of Biology, University of Florida, Gainesville, Florida 32611, USA [2] Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA [3] Genetics Institute, University of Florida, Gainesville, Florida 32611, USA.
authors.forename: Douglas E
authors.initials: DE
authors.lastname: Soltis
authors.affiliation: Department of Biology, University of Missouri-St Louis, St Louis, Missouri 63121, USA.
authors.forename: Peter F
authors.initials: PF
authors.lastname: Stevens
authors.affiliation: Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia.
authors.forename: Mark
authors.initials: M
authors.lastname: Westoby
authors.affiliation: Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia.
authors.forename: Ian J
authors.initials: IJ
authors.lastname: Wright
authors.affiliation: Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada.
authors.forename: Lonnie
authors.initials: L
authors.lastname: Aarssen
authors.affiliation: Department of Biology, College of the Holy Cross, Worcester, Massachusetts 01610, USA.
authors.forename: Robert I
authors.initials: RI
authors.lastname: Bertin
authors.affiliation: Department of Biology, University of Florida, Gainesville, Florida 32611, USA.
authors.forename: Andre
authors.initials: A
authors.lastname: Calaminus
authors.affiliation: Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, United Kingdom.
authors.forename: Rafaël
authors.initials: R
authors.lastname: Govaerts
authors.affiliation: Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia.
authors.forename: Frank
authors.initials: F
authors.lastname: Hemmings
authors.affiliation: Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia.
authors.forename: Michelle R
authors.initials: MR
authors.lastname: Leishman
authors.affiliation: 1] Department of Forest Resources, University of Minnesota, St Paul, Minnesota 55108, USA [2] Polish Academy of Sciences, Institute of Dendrology, 62-035 Kornik, Poland.
authors.forename: Jacek
authors.initials: J
authors.lastname: Oleksyn
authors.affiliation: 1] Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, USA [2] Genetics Institute, University of Florida, Gainesville, Florida 32611, USA.
authors.forename: Pamela S
authors.initials: PS
authors.lastname: Soltis
authors.affiliation: Department of Plant Biology and Ecology, Evolutionary Biology and Behavior, Program, Michigan State University, East Lansing, Michigan 48824, USA.
authors.forename: Nathan G
authors.initials: NG
authors.lastname: Swenson
authors.affiliation: 1] Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia [2] Institute of Pacific Islands Forestry, USDA Forest Service, Hilo, Hawaii 96720, USA.
authors.forename: Laura
authors.initials: L
authors.lastname: Warman
authors.affiliation: National Institute for Mathematical & Biological Synthesis, University of Tennessee, Knoxville, Tennessee 37996, USA.
authors.forename: Jeremy M
authors.initials: JM
authors.lastname: Beaulieu
mesh_terms: D005075:Biological Evolution; D003081:Cold Climate; D017753:Ecosystem; D005615:Freezing; D016013:Likelihood Functions; D019684:Magnoliopsida / Q000033:anatomy & histology* / Q000502:physiology*; D058974:Phylogeography; D018515:Plant Leaves / Q000033:anatomy & histology / Q000502:physiology; D012639:Seeds / Q000502:physiology; D013997:Time Factors; D014934:Wood / Q000033:anatomy & histology / Q000502:physiology; D052584:Xylem / Q000033:anatomy & histology* / Q000502:physiology