Paleotemperature Proxies from Leaf Fossils Reinterpreted in Light of Evolutionary History

Stefan A Little,Peter Wilf,Steven W Kembel,Andrew Allen Farke

doi:10.1371/journal.pone.0015161

Stefan A Little, Peter Wilf + Show 2 more

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https://doi.org/10.1371/journal.pone.0015161

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Abstract

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.

Highlights

In a seminal 1915 paper, Bailey and Sinnott proposed ‘‘a botanical index of Cretaceous and Tertiary climates’’ [1]: in extant mesic floras, the proportion of woody ‘‘dicot’’ species that have untoothed leaf margins (NT) is positively related to mean annual temperature (MAT), and quantifying untoothed taxa in fossil floras is informative about past temperatures
All trait-climate regression models were improved by incorporation of phylogenetic relationships (Table 1; Figure 2), as demonstrated by the much lower Akaike Information Criterion (AIC) scores for phylogenetic generalized least squares (GLS) versus non-phylogenetic GLS models for all traits
The standard errors of the intercepts in pGLS regressions were generally higher than in non-phylogenetic GLS regressions (Table 1), leading to greater uncertainty in predictions of climate after phylogenetic relationships are taken into account

Summary

Introduction

In a seminal 1915 paper, Bailey and Sinnott proposed ‘‘a botanical index of Cretaceous and Tertiary climates’’ [1]: in extant mesic floras, the proportion of woody ‘‘dicot’’ species that have untoothed leaf margins (NT) is positively related to mean annual temperature (MAT), and quantifying untoothed taxa in fossil floras is informative about past temperatures. Because this relationship occurs across different continents and biomes containing various plant lineages, the authors suggested that environmental convergence is the most important explanatory factor, rather than phylogenetic causes [1,2]. The general, often-stated consensus (but see below) is that the climatic distribution of leaf physiognomic traits should be similar in the past and that phylogeny is a negligible component

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