William K. Cornwell

Three keys to the radiation of angiosperms into freezing environments

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.

The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change

Species are the unit of analysis in many global change and conservation biology studies; however, species are not uniform entities but are composed of different, sometimes locally adapted, populations differing in plasticity. We examined how intraspecific variation in thermal niches and phenotypic plasticity will affect species distributions in a warming climate. We first developed a conceptual model linking plasticity and niche breadth, providing five alternative intraspecific scenarios that are consistent with existing literature. Secondly, we used ecological niche-modeling techniques to quantify the impact of each intraspecific scenario on the distribution of a virtual species across a geographically realistic setting. Finally, we performed an analogous modeling exercise using real data on the climatic niches of different tree provenances. We show that when population differentiation is accounted for and dispersal is restricted, forecasts of species range shifts under climate change are even more pessimistic than those using the conventional assumption of homogeneously high plasticity across a species range. Suitable population-level data are not available for most species so identifying general patterns of population differentiation could fill this gap. However, the literature review revealed contrasting patterns among species, urging greater levels of integration among empirical, modeling and theoretical research on intraspecific phenotypic variation.

A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms

Symbiotic associations occur in every habitat on earth, but we know very little about their evolutionary histories. Current models of trait evolution cannot adequately reconstruct the deep history of symbiotic innovation, because they assume homogenous evolutionary processes across millions of years. Here we use a recently developed, heterogeneous and quantitative phylogenetic framework to study the origin of the symbiosis between angiosperms and nitrogen-fixing (N2) bacterial symbionts housed in nodules. We compile the largest database of global nodulating plant species and reconstruct the symbiosis’ evolution. We identify a single, cryptic evolutionary innovation driving symbiotic N2-fixation evolution, followed by multiple gains and losses of the symbiosis, and the subsequent emergence of ‘stable fixers’ (clades extremely unlikely to lose the symbiosis). Originating over 100 MYA, this innovation suggests deep homology in symbiotic N2-fixation. Identifying cryptic innovations on the tree of life is key to understanding the evolution of complex traits, including symbiotic partnerships.

Functional distinctiveness of major plant lineages

Summary nPlant traits vary widely across species and underpin differences in ecological strategy. Despite centuries of interest, the contributions of different evolutionary lineages to modern-day functional diversity remain poorly quantified. nExpanding data bases of plant traits plus rapidly improving phylogenies enable for the first time a data-driven global picture of plant functional diversity across the major clades of higher plants. We mapped five key traits relevant to metabolism, resource competition and reproductive strategy onto a phylogeny across 48324 vascular plant species world-wide, along with climate and biogeographic data. Using a novel metric, we test whether major plant lineages are functionally distinctive. We then highlight the trait–lineage combinations that are most functionally distinctive within the present-day spread of ecological strategies. nFor some trait–clade combinations, knowing the clade of a species conveys little information to neo- and palaeo-ecologists. In other trait–clade combinations, the clade identity can be highly revealing, especially informative clade–trait combinations include Proteaceae, which is highly distinctive, representing the global slow extreme of the leaf economic spectrum. Magnoliidae and Rosidae contribute large leaf sizes and seed masses and have distinctively warm, wet climatic distributions. nSynthesis. This analysis provides a shortlist of the most distinctive trait–lineage combinations along with their geographic and climatic context: a global view of extant functional diversity across the tips of the vascular plant phylogeny.

Model Adequacy and the Macroevolution of Angiosperm Functional Traits.

Making meaningful inferences from phylogenetic comparative data requires a meaningful model of trait evolution. It is thus important to determine whether the model is appropriate for the data and the question being addressed. One way to assess this is to ask whether the model provides a good statistical explanation for the variation in the data. To date, researchers have focused primarily on the explanatory power of a model relative to alternative models. Methods have been developed to assess the adequacy, or absolute explanatory power, of phylogenetic trait models, but these have been restricted to specific models or questions. Here we present a general statistical framework for assessing the adequacy of phylogenetic trait models. We use our approach to evaluate the statistical performance of commonly used trait models on 337 comparative data sets covering three key angiosperm functional traits. In general, the models we tested often provided poor statistical explanations for the evolution of these traits. This was true for many different groups and at many different scales. Whether such statistical inadequacy will qualitatively alter inferences drawn from comparative data sets will depend on the context. Regardless, assessing model adequacy can provide interesting biological insights—how and why a model fails to describe variation in a data set give us clues about what evolutionary processes may have driven trait evolution across time.

How much of the world is woody

Summary 1. The question posed by the title of this study is a basic one, and it is surprising that the answer is not known. Recently, assembled trait data sets provide an opportunity to address this, but scaling these data sets to the global scale is challenging because of sampling bias. Although we currently know the growth form of tens of thousands of species, these data are not a random sample of global diversity; some clades are exhaustively characterized, while others we know little to nothing about. 2. Starting with a data base of woodiness for 39 313 species of vascular plants (12% of taxonomically resolved species, 59% of which were woody), we estimated the status of the remaining taxonomically resolved species by randomization. To compare the results of our method to conventional wisdom, we informally surveyed a broad community of biologists. No consensus answer to the question existed, with estimates ranging from 1% to 90% (mean: 31.7%). 3. After accounting for sampling bias, we estimated the proportion of woodiness among the world’s vascular plants to be between 45% and 48%. This was much lower than a simple mean of our data set and much higher than the conventional wisdom. 4. Synthesis. Alongside an understanding of global taxonomic diversity (i.e. number of species globally), building a functional understanding of global diversity is an important emerging research direction. This approach represents a novel way to account for sampling bias in functional trait data sets and to answer basic questions about functional diversity at a global scale.

A global method for calculating plant CSR ecological strategies applied across biomes world‐wide

Summary nCompetitor, stress-tolerator, ruderal (CSR) theory is a prominent plant functional strategy scheme previously applied to local floras. Globally, the wide geographic and phylogenetic coverage of available values of leaf area (LA), leaf dry matter content (LDMC) and specific leaf area (SLA) (representing, respectively, interspecific variation in plant size and conservative vs. acquisitive resource economics) promises the general application of CSR strategies across biomes, including the tropical forests hosting a large proportion of Earths diversity. nWe used trait variation for 3068 tracheophytes (representing 198 families, six continents and 14 biomes) to create a globally calibrated CSR strategy calculator tool and investigate strategy–environment relationships across biomes world-wide. nDue to disparity in trait availability globally, co-inertia analysis was used to check correspondence between a ‘wide geographic coverage, few traits’ data set and a ‘restricted coverage, many traits’ subset of 371 species for which 14 whole-plant, flowering, seed and leaf traits (including leaf nitrogen content) were available. CSR strategy/environment relationships within biomes were investigated using fourth-corner and RLQ analyses to determine strategy/climate specializations. nStrong, significant concordance (RVxa0=xa00·597; Pxa0<xa00·0001) was evident between the 14 trait multivariate space and when only LA, LDMC and SLA were used. nBiomes such as tropical moist broadleaf forests exhibited strategy convergence (i.e. clustered around a CS/CSR median; C:S:Rxa0=xa043:42:15%), with CS-selection associated with warm, stable situations (lesser temperature seasonality), with greater annual precipitation and potential evapotranspiration. Other biomes were characterized by strategy divergence: for example, deserts varied between xeromorphic perennials such as Larrea divaricata, classified as S-selected (C:S:Rxa0=xa01:99:0%) and broadly R-selected annual herbs (e.g. Claytonia perfoliata; R/CR-selected; C:S:Rxa0=xa021:0:79%). Strategy convergence was evident for several growth habits (e.g. trees) but not others (forbs). nThe CSR strategies of vascular plants can now be compared quantitatively within and between biomes at the global scale. Through known linkages between underlying leaf traits and growth rates, herbivory and decomposition rates, this method and the strategy–environment relationships it elucidates will help to predict which kinds of species may assemble in response to changes in biogeochemical cycles, climate and land use.

Trees, branches and (square) roots: why evolutionary relatedness is not linearly related to functional distance

Summary nAn increasingly popular practice in community ecology is to use the evolutionary distance among interacting species as a proxy for their overall functional similarity. nAt the core of this approach is the implicit, yet poorly recognized, assumption that trait dissimilarity increases linearly with divergence time, that is all evolutionary time is considered equal. However, given a classic Brownian model of trait evolution, we show that the expected functional displacement of any two taxa is more appropriately represented as a linear function of times square root. nIn light of this mismatch between theory and methodology, we argue that current methods at the interface of ecology and evolutionary biology often greatly overweight deep time relative to recent time. nAn easy solution to this weighting problem is a square root transformation of the phylogenetic distance matrix. Using simulated models of trait evolution and community assembly, we show that this transformation yields considerably higher statistical power, with improvements in 92% of trials. This methodological update is likely to improve our understanding of the connection between evolutionary relatedness and contemporary ecological processes.

Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis

Mutualistic symbioses with mycorrhizal fungi are widespread in plants. The majority of plant species associate with arbuscular mycorrhizal (AM) fungi. By contrast, the minority associate with ectomycorrhizal (EM) fungi, have abandoned the symbiosis and are nonmycorrhizal (NM), or engage in an intermediate, weakly AM symbiosis (AMNM). To understand the processes that maintain the mycorrhizal symbiosis or cause its loss, we reconstructed its evolution using a ∼3,000-species seed plant phylogeny integrated with mycorrhizal state information. Reconstruction indicated that the common ancestor of seed plants most likely associated with AM fungi and that the EM, NM, and AMNM states descended from the AM state. Direct transitions from the AM state to the EM and NM states were infrequent and generally irreversible, implying that natural selection or genetic constraint could promote stasis once a particular state evolved. However, the evolution of the NM state was more frequent via an indirect pathway through the AMNM state, suggesting that weakening of the AM symbiosis is a necessary precursor to mutualism abandonment. Nevertheless, reversions from the AMNM state back to the AM state were an order of magnitude more likely than transitions to the NM state, suggesting that natural selection favors the AM symbiosis over mutualism abandonment.

Flammability across the gymnosperm phylogeny: the importance of litter particle size

Fire is important to climate, element cycles and plant communities, with many fires spreading via surface litter. The influence of species on the spread of surface fire is mediated by their traits which, after senescence and abscission, have afterlife effects on litter flammability. We hypothesized that differences in litter flammability among gymnosperms are determined by litter particle size effects on litterbed packing. We performed a mesocosm fire experiment comparing 39 phylogenetically wide-ranging gymnosperms, followed by litter size and shape manipulations on two chemically contrasting species, to isolate the underlying mechanism. The first-order control on litter flammability was, indeed, litter particle size in both experiments. Most gymnosperms were highly flammable, but a prominent exception was the non-Pinus Pinaceae, in which small leaves abscised singly produced dense, non-flammable litterbeds. There are two important implications: first, ecosystems dominated by gymnosperms that drop small leaves separately will develop dense litter layers, which will be less prone to and inhibit the spread of surface litter fire. Second, some of the needle-leaved species previously considered to be flammable in single-leaf experiments were among the least flammable in litter fuel beds, highlighting the role of the litter traits of species in affecting surface fire regimes.