Insights on the evolution of plant succulence from a remarkable radiation in Madagascar (Euphorbia).
Patterns of adaptation in response to environmental variation are central to our understanding of biodiversity, but predictions of how and when broad-scale environmental conditions such as climate affect organismal form and function remain incomplete. Succulent plants have evolved in response to arid conditions repeatedly, with various plant organs such as leaves, stems, and roots physically modified to increase water storage. Here, we investigate the role played by climate conditions in shaping the evolution of succulent forms in a plant clade endemic to Madagascar and the surrounding islands, part of the hyper-diverse genus Euphorbia (Euphorbiaceae). We used multivariate ordination of 19 climate variables to identify links between particular climate variables and three major forms of succulence-succulent leaves, cactiform stem succulence, and tubers. We then tested the relationship between climatic conditions and succulence, using comparative methods that account for shared evolutionary history. We confirm that plant water storage is associated with the two components of aridity, temperature, and precipitation. Cactiform stem succulence, however, is not prevalent in the driest environments, countering the widely held view of cactiforms as desert icons. Instead, leaf succulence and tubers are significantly associated with the lowest levels of precipitation. Our findings provide a clear link between broad-scale climatic conditions and adaptation in land plants, and new insights into the climatic conditions favoring different forms of succulence. This evidence for adaptation to climate raises concern over the evolutionary future of succulent plants as they, along with other organisms, face anthropogenic climate change.
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USALaboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USALaboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoi
Margaret
M
Evans
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USALaboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
Xavier
X
Aubriot
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
David
D
Hearn
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
Maxime
M
Lanciaux
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
Sebastien
S
Lavergne
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
Corinne
C
Cruaud
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USALaboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
Porter P
PP
Lowry
Laboratory of Tree-Ring Research, 1215 E Lowell Street and Department of Ecology and Evolutionary Biology, 1041 E Lowell Street, University of Arizona, Tucson, AZ 85721, USA ISYEB, Institut de Systématique, Évolution, Biodiversité (UMR 7205 CNRS, MNHN, EPHE, UPMC), Muséum national d'histoire naturelle, National Herbarium, CP 39, 57 rue Cuvier, 75231 Paris Cedex 05, France Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Biological Sciences, Towson University, 8000 York Rd, Baltimore, MD 21252, USA Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, Grenoble I, BP 53, 38041 Grenoble Cedex 9, France Genoscope, Centre National de Sequençage, CP5706, 2 rue Gaston Crémieux, 91057 Evry Cedex, France; and Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA.
Thomas
T
Haevermans
D044822:Biodiversity; D002980:Climate; D028481:Euphorbia / Q000145:classification* / Q000235:genetics / Q000502:physiology*; D005819:Genetic Markers / Q000235:genetics; D049810:Genetic Speciation; D008270:Madagascar; D010802:Phylogeny; D018515:Plant Leaves / Q000502:physiology
D005819:Genetic Markers