Richard G. FitzJohn

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.

Estimating Trait-Dependent Speciation and Extinction Rates from Incompletely Resolved Phylogenies

Species traits may influence rates of speciation and extinction, affecting both the patterns of diversification among lineages and the distribution of traits among species. Existing likelihood approaches for detecting differential diversification require complete phylogenies; that is, every extant species must be present in a well-resolved phylogeny. We developed 2 likelihood methods that can be used to infer the effect of a trait on speciation and extinction without complete phylogenetic information, generalizing the recent binary-state speciation and extinction method. Our approaches can be used where a phylogeny can be reasonably assumed to be a random sample of extant species or where all extant species are included but some are assigned only to terminal unresolved clades. We explored the effects of decreasing phylogenetic resolution on the ability of our approach to detect differential diversification within a Bayesian framework using simulated phylogenies. Differential diversification caused by an asymmetry in speciation rates was nearly as well detected with only 50% of extant species phylogenetically resolved as with complete phylogenetic knowledge. We demonstrate our unresolved clade method with an analysis of sexual dimorphism and diversification in shorebirds (Charadriiformes). Our methods allow for the direct estimation of the effect of a trait on speciation and extinction rates using incompletely resolved phylogenies.

The Unsolved Challenge to Phylogenetic Correlation Tests for Categorical Characters

1Departments of Zoology and Botany and Beaty Biodiversity Museum, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z4; 2Departments of Zoology and Biodiversity Research Centre, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z4 and 3Department of Biological Sciences, Macquarie University, Sydney NSW 2109, Australia ∗Correspondence to be sent to: Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z4; E-mail: wayne.maddison@ubc.ca.

Quantitative Traits and Diversification

Quantitative traits have long been hypothesized to affect speciation and extinction rates. For example, smaller body size or increased specialization may be associated with increased rates of diversification. Here, I present a phylogenetic likelihood-based method (quantitative state speciation and extinction [QuaSSE]) that can be used to test such hypotheses using extant character distributions. This approach assumes that diversification follows a birth-death process where speciation and extinction rates may vary with one or more traits that evolve under a diffusion model. Speciation and extinction rates may be arbitrary functions of the character state, allowing much flexibility in testing models of trait-dependent diversification. I test the approach using simulated phylogenies and show that a known relationship between speciation and a quantitative character could be recovered in up to 80% of the cases on large trees (500 species). Consistent with other approaches, detecting shifts in diversification due to differences in extinction rates was harder than when due to differences in speciation rates. Finally, I demonstrate the application of QuaSSE to investigate the correlation between body size and diversification in primates, concluding that clade-specific differences in diversification may be more important than size-dependent diversification in shaping the patterns of diversity within this group.

Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review

Terminal restriction fragment length polymorphism (T-RFLP) is an increasingly widely used technique in mycorrhizal ecology. In this paper, we review the technique as it is used to identify species of mycorrhizal fungi and distinguish two different versions of the technique: peak-profile T-RFLP (the original version) and database T-RFLP. We define database T-RFLP as the use of T-RFLP to identify individual species within samples by comparison of unknown data with a database of known T-RFLP patterns. This application of T-RFLP avoids some of the pitfalls of peak-profile T-RFLP and allows T-RFLP to be applied to polyphyletic functional groups such as ectomycorrhizal fungi. The identification of species using database T-RFLP is subject to several sources of potential error, including (1) random erroneous matches of peaks to species, (2) shared T-RFLP profiles across species, and (3) multiple T-RFLP profiles within a species. A mathematical approximation of the risk of the first type of error as a function of experimental parameters is discussed. Although potentially less accurate than some other methods such as clone libraries, the high throughput of database T-RFLP permits much greater replication and may, therefore, be preferable for many ecological questions, particularly when combined with other techniques such as cloning.

geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees

SUMMARY Phylogenetic comparative methods are essential for addressing evolutionary hypotheses with interspecific data. The scale and scope of such data have increased dramatically in the past few years. Many existing approaches are either computationally infeasible or inappropriate for data of this size. To address both of these problems, we present geiger v2.0, a complete overhaul of the popular R package geiger. We have reimplemented existing methods with more efficient algorithms and have developed several new approaches for accomodating heterogeneous models and data types. AVAILABILITY AND IMPLEMENTATION  This R package is available on the CRAN repository http://cran.r-project.org/web/packages/geiger/. All source code is also available on github http://github.com/mwpennell/geiger-v2. geiger v2.0 depends on the ape package. CONTACT mwpennell@gmail.com SUPPLEMENTARY INFORMATION  Supplementary data are available at Bioinformatics online.

Functional distinctiveness of major plant lineages

Summary Plant 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. Expanding 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. For 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. Synthesis. 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.

Loss of sexual recombination and segregation is associated with increased diversification in evening primroses.

The loss of sexual recombination and segregation in asexual organisms has been portrayed as an irreversible process that commits asexually reproducing lineages to reduced diversification. We test this hypothesis by estimating rates of speciation, extinction, and transition between sexuality and functional asexuality in the evening primroses. Specifically, we estimate these rates using the recently developed BiSSE (Binary State Speciation and Extinction) phylogenetic comparative method, which employs maximum likelihood and Bayesian techniques. We infer that net diversification rates (speciation minus extinction) in functionally asexual evening primrose lineages are roughly eight times faster than diversification rates in sexual lineages, largely due to higher speciation rates in asexual lineages. We further reject the hypothesis that a loss of recombination and segregation is irreversible because the transition rate from functional asexuality to sexuality is significantly greater than zero and in fact exceeded the reverse rate. These results provide the first empirical evidence in support of the alternative theoretical prediction that asexual populations should instead diversify more rapidly than sexual populations because they are free from the homogenizing effects of sexual recombination and segregation. Although asexual reproduction may often constrain adaptive evolution, our results show that the loss of recombination and segregation need not be an evolutionary dead end in terms of diversification of lineages.

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.