Paleotemperature Proxies from Leaf Fossils Reinterpreted in Light of Evolutionary History

Present-day correlations between leaf physiognomic traits (shape and size) and climate are widely used to estimate paleoclimate using fossil floras. For example, leaf-margin analysis estimates paleotemperature using the modern relation of mean annual temperature (MAT) and the site-proportion of untoothed-leaf species (NT). This uniformitarian approach should provide accurate paleoclimate reconstructions under the core assumption that leaf-trait variation principally results from adaptive environmental convergence, and because variation is thus largely independent of phylogeny it should be constant through geologic time. Although much research acknowledges and investigates possible pitfalls in paleoclimate estimation based on leaf physiognomy, the core assumption has never been explicitly tested in a phylogenetic comparative framework. Combining an extant dataset of 21 leaf traits and temperature with a phylogenetic hypothesis for 569 species-site pairs at 17 sites, we found varying amounts of non-random phylogenetic signal in all traits. Phylogenetic vs. standard regressions generally support prevailing ideas that leaf-traits are adaptively responding to temperature, but wider confidence intervals, and shifts in slope and intercept, indicate an overall reduced ability to predict climate precisely due to the non-random phylogenetic signal. Notably, the modern-day relation of proportion of untoothed taxa with mean annual temperature (NT-MAT), central in paleotemperature inference, was greatly modified and reduced, indicating that the modern correlation primarily results from biogeographic history. Importantly, some tooth traits, such as number of teeth, had similar or steeper slopes after taking phylogeny into account, suggesting that leaf teeth display a pattern of exaptive evolution in higher latitudes. This study shows that the assumption of convergence required for precise, quantitative temperature estimates using present-day leaf traits is not supported by empirical evidence, and thus we have very low confidence in previously published, numerical paleotemperature estimates. However, interpreting qualitative changes in paleotemperature remains warranted, given certain conditions such as stratigraphically closely-spaced samples with floristic continuity.

[1]  F. Pérez,et al.  Historical and phylogenetic constraints on the incidence of entire leaf margins: insights from a new South American model , 2011 .

[2]  Nathan J B Kraft,et al.  Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. , 2011, The New phytologist.

[3]  C. Labandeira,et al.  Fossil insect folivory tracks paleotemperature for six million years , 2010 .

[4]  T. Casci Population genetics: Breaking down hybrids , 2010, Nature Reviews Genetics.

[5]  Christian Peter Klingenberg,et al.  Evolution and development of shape: integrating quantitative approaches , 2010, Nature Reviews Genetics.

[6]  T. Casci Gene regulation: Small ORFs conceal bioactive peptides , 2010, Nature Reviews Genetics.

[7]  Guido Sanguinetti,et al.  LEAFPROCESSOR: a new leaf phenotyping tool using contour bending energy and shape cluster analysis. , 2010, The New phytologist.

[8]  Campbell O. Webb,et al.  Picante: R tools for integrating phylogenies and ecology , 2010, Bioinform..

[9]  D. Royer,et al.  Quantification of large uncertainties in fossil leaf paleoaltimetry , 2010 .

[10]  K. Oyama,et al.  Leaf Fluctuating Asymmetry Increases with Hybridization and Introgression between Quercus magnoliifolia and Quercus resinosa (Fagaceae) through an Altitudinal Gradient in Mexico , 2010, International Journal of Plant Sciences.

[11]  R. C. Keating Manual of Leaf Architecture , 2009 .

[12]  P. Valdes,et al.  New developments in CLAMP: Calibration using global gridded meteorological data , 2009 .

[13]  K. Robertson,et al.  Phenotypic Plasticity of Leaf Shape along a Temperature Gradient in Acer rubrum , 2009, PloS one.

[14]  Maria A. Gandolfo,et al.  Phylogenetic biome conservatism on a global scale , 2009, Nature.

[15]  J. Chave,et al.  Towards a Worldwide Wood Economics Spectrum 2 . L E a D I N G D I M E N S I O N S I N W O O D F U N C T I O N , 2022 .

[16]  D. Royer,et al.  Ecology of Leaf Teeth: a Multi-site Analysis from an Australian Subtropical Rainforest 1 , 2022 .

[17]  D. Royer,et al.  Sensitivity of leaf size and shape to climate within Acer rubrum and Quercus kelloggii. , 2008, The New phytologist.

[18]  J. Trygg,et al.  LAMINA: a tool for rapid quantification of leaf size and shape parameters , 2008, BMC Plant Biology.

[19]  Campbell O. Webb,et al.  Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. , 2008, Ecology.

[20]  M. Aizen,et al.  Do leaf margins of the temperate forest flora of southern South America reflect a warmer past , 2008 .

[21]  José Luis Micol,et al.  Mutational spaces for leaf shape and size , 2008, HFSP journal.

[22]  Yang-jian Zhang,et al.  Leaf margins and temperature in the North American flora: Recalibrating the paleoclimatic thermometer , 2008 .

[23]  Luke J. Harmon,et al.  GEIGER: investigating evolutionary radiations , 2008, Bioinform..

[24]  Campbell O. Webb,et al.  Relationships among ecologically important dimensions of plant trait variation in seven neotropical forests. , 2007, Annals of botany.

[25]  R. Guralnick,et al.  GENERATING EMPIRICALLY DETERMINED, CONTINUOUS MEASURES OF LEAF SHAPE FOR PALEOCLIMATE RECONSTRUCTION , 2007 .

[26]  D. Greenwood Fossil angiosperm leaves and climate: from Wolfe and Dilcher to Burnham and Wilf , 2007 .

[27]  L. Hickey,et al.  Using leaf margin analysis to estimate the mid-Cretaceous (Albian) paleolatitude of the Baja BC block , 2006 .

[28]  C. Villagrán,et al.  Are Chilean coastal forests pre‐Pleistocene relicts? Evidence from foliar physiognomy, palaeoclimate, and phytogeography , 2006 .

[29]  D. Royer,et al.  Why Do Toothed Leaves Correlate with Cold Climates? Gas Exchange at Leaf Margins Provides New Insights into a Classic Paleotemperature Proxy , 2006, International Journal of Plant Sciences.

[30]  W. Green LOOSENING THE CLAMP: AN EXPLORATORY GRAPHICAL APPROACH TO THE CLIMATE LEAF ANALYSIS MULTIVARIATE PROGRAM , 2006 .

[31]  Scott L Wing,et al.  Transient Floral Change and Rapid Global Warming at the Paleocene-Eocene Boundary , 2005, Science.

[32]  T. Feild,et al.  Hydathodal leaf teeth of Chloranthus japonicus (Chloranthaceae) prevent guttation‐induced flooding of the mesophyll , 2005 .

[33]  D. Royer,et al.  Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. , 2005, American journal of botany.

[34]  D. Cantrill,et al.  A multi-proxy approach to determine Antarctic terrestrial palaeoclimate during the Late Cretaceous and Early Tertiary , 2005 .

[35]  T. Feild,et al.  Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossils. , 2005, The New phytologist.

[36]  Campbell O. Webb,et al.  Phylomatic: tree assembly for applied phylogenetics , 2005 .

[37]  S. Wing,et al.  Oxygen isotope and paleobotanical estimates of temperature and δ18O–latitude gradients over North America during the early Eocene , 2004 .

[38]  D. Greenwood,et al.  Paleotemperature Estimation Using Leaf-Margin Analysis: Is Australia Different? , 2004 .

[39]  Pamela S Soltis,et al.  Darwin's abominable mystery: Insights from a supertree of the angiosperms , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[41]  V. Mosbrugger,et al.  Testing the climatic estimates from different palaeobotanical methods: an example from the Middle Miocene Shanwang flora of China , 2003 .

[42]  V. Mosbrugger,et al.  Reconstructing palaeotemperatures using leaf floras – case studies for a comparison of leaf margin analysis and the coexistence approach , 2003 .

[43]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[44]  P. Wilf,et al.  Digital Future for Paleoclimate Estimation from Fossil Leaves? Preliminary Results , 2003 .

[45]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[46]  Christina Gloeckner,et al.  Modern Applied Statistics With S , 2003 .

[47]  Kirk R. Johnson,et al.  Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous–Paleogene boundary , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[48]  I. Poole,et al.  Paleogene West Antarctic climate and vegetation history in light of new data from King George Island , 2003 .

[49]  Elizabeth A. Kowalski Mean annual temperature estimation based on leaf morphology: a test from tropical South America , 2002 .

[50]  T. Garland,et al.  Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods , 2002 .

[51]  N. Pitman,et al.  Habitat-related error in estimating temperatures from leaf margins in a humid tropical forest. , 2001, American journal of botany.

[52]  V. Mosbrugger,et al.  Terrestrial Climate Evolution in Northwest Germany Over the Last 25 Million Years , 2000 .

[53]  P. Wilf Late Paleocene–early Eocene climate changes in southwestern Wyoming: Paleobotanical analysis , 2000 .

[54]  S. Wing,et al.  Warm Climates in Earth History: Index , 1999 .

[55]  M. Pagel Inferring the historical patterns of biological evolution , 1999, Nature.

[56]  J. Basinger,et al.  EARLY TERTIARY FLORAL EVOLUTION IN THE CANADIAN HIGH ARCTIC , 1999 .

[57]  S. Manchester Biogeographical Relationships of North American Tertiary Floras , 1999 .

[58]  P. Koch,et al.  Warm Climates in Earth History: An early Eocene cool period? Evidence for ceontinental cooling during the warmest part of the Cenozoic , 1999 .

[59]  S. Wing,et al.  Attached leaves and fruits of myrtaceous affinity from the Middle Eocene of Colorado , 1998 .

[60]  R. Burnham Stand Characteristics and Leaf Litter Composition of a Dry Forest Hectare in Santa Rosa National Park, Costa Rica , 1997 .

[61]  V. Mosbrugger,et al.  The coexistence approach — a method for quantitative reconstructions of Tertiary terrestrial palaeoclimate data using plant fossils , 1997 .

[62]  P. Wilf When are leaves good thermometers? A new case for Leaf Margin Analysis , 1997, Paleobiology.

[63]  P. England,et al.  The use of a resemblance function in the measurement of climatic parameters from the physiognomy of woody dicotyledons , 1997 .

[64]  G. Jordan Uncertainty in palaeoclimatic reconstructions based on leaf physiognomy , 1997 .

[65]  D. Greenwood,et al.  Eocene continental climates and latitudinal temperature gradients: Comment and Reply , 1996 .

[66]  D. Greenwood,et al.  Eocene continental climates and latitudinal temperature gradients , 1995 .

[67]  J. A. Wolfe PALEOCLIMATIC ESTIMATES FROM TERTIARY LEAF ASSEMBLAGES , 1995 .

[68]  D. Greenwood,et al.  Fossils and fossil climate: the case for equable continental interiors in the Eocene , 1993 .

[69]  J. A. Wolfe A method of obtaining climatic parameters from leaf assemblages , 1993 .

[70]  W. G. Chaloner,et al.  Do fossil plants give a climatic signal? , 1990, Journal of the Geological Society.

[71]  A. Grafen The phylogenetic regression. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[72]  J. A. Wolfe Late Cretaceous-Cenozoic history of deciduousness and the terminal Cretaceous event , 1987, Paleobiology.

[73]  J. A. Wolfe,et al.  North American nonmarine climates and vegetation during the Late Cretaceous , 1987 .

[74]  S. Wing Eocene and Oligocene Floras and Vegetation of the Rocky Mountains , 1987 .

[75]  J. A. Wolfe,et al.  Vegetation, climatic and floral changes at the Cretaceous-Tertiary boundary , 1986, Nature.

[76]  W. Berger,et al.  Climate in Earth history , 1982 .

[77]  J. A. Wolfe Temperature parameters of humid to mesic forests of Eastern Asia and relation to forests of other regions of the Northern Hemisphere and Australasia: analysis of temperature data from more than 400 stations in Eastern Asia , 1979 .

[78]  Leo J. Hickey,et al.  The bases of angiosperm phylogeny: vegetative morphology. , 1975 .

[79]  A. Graham,et al.  Vegetation and Vegetational History of Northern Latin America. , 1975 .

[80]  J. A. Wolfe Tertiary climatic fluctuations and methods of analysis of tertiary floras , 1971 .

[81]  J. A. Wolfe Tertiary plants from the Cook Inlet region, Alaska , 1966 .

[82]  E. W. Sinnott,et al.  THE CLIMATIC DISTRIBUTION OF CERTAIN TYPES OF ANGIOSPERM LEAVES , 1916 .

[83]  E. W. Sinnott,et al.  A BOTANICAL INDEX OF CRETACEOUS AND TERTIARY CLIMATES. , 1915, Science.

[84]  A. Classen,et al.  Leaf form and the reconstruction of past climates , 2022 .