Jonathan M. Eastman

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.

Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data

Understanding the evolutionary history of microbial pathogens is critical for mitigating the impacts of emerging infectious diseases on economically and ecologically important host species. We used a genome resequencing approach to resolve the evolutionary history of an important microbial pathogen, the chytrid Batrachochytrium dendrobatidis (Bd), which has been implicated in amphibian declines worldwide. We sequenced the genomes of 29 isolates of Bd from around the world, with an emphasis on North, Central, and South America because of the devastating effect that Bd has had on amphibian populations in the New World. We found a substantial amount of evolutionary complexity in Bd with deep phylogenetic diversity that predates observed global amphibian declines. By investigating the entire genome, we found that even the most recently evolved Bd clade (termed the global panzootic lineage) contained more genetic variation than previously reported. We also found dramatic differences among isolates and among genomic regions in chromosomal copy number and patterns of heterozygosity, suggesting complex and heterogeneous genome dynamics. Finally, we report evidence for selection acting on the Bd genome, supporting the hypothesis that protease genes are important in evolutionary transitions in this group. Bd is considered an emerging pathogen because of its recent effects on amphibians, but our data indicate that it has a complex evolutionary history that predates recent disease outbreaks. Therefore, it is important to consider the contemporary effects of Bd in a broader evolutionary context and identify specific mechanisms that may have led to shifts in virulence in this system.

A NOVEL COMPARATIVE METHOD FOR IDENTIFYING SHIFTS IN THE RATE OF CHARACTER EVOLUTION ON TREES

Evolutionary biologists since Darwin have been fascinated by differences in the rate of trait‐evolutionary change across lineages. Despite this continued interest, we still lack methods for identifying shifts in evolutionary rates on the growing tree of life while accommodating uncertainty in the evolutionary process. Here we introduce a Bayesian approach for identifying complex patterns in the evolution of continuous traits. The method (auteur) uses reversible‐jump Markov chain Monte Carlo sampling to more fully characterize the complexity of trait evolution, considering models that range in complexity from those with a single global rate to potentially ones in which each branch in the tree has its own independent rate. This newly introduced approach performs well in recovering simulated rate shifts and simulated rates for datasets nearing the size typical for comparative phylogenetic study (i.e., ≥64 tips). Analysis of two large empirical datasets of vertebrate body size reveal overwhelming support for multiple‐rate models of evolution, and we observe exceptionally high rates of body‐size evolution in a group of emydid turtles relative to their evolutionary background. auteur will facilitate identification of exceptional evolutionary dynamics, essential to the study of both adaptive radiation and stasis.

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.

Goldilocks Meets Santa Rosalia: An Ephemeral Speciation Model Explains Patterns of Diversification Across Time Scales

Understanding the rate at which new species form is a key question in studying the evolution of life on earth. Here we review our current understanding of speciation rates, focusing on studies based on the fossil record, phylogenies, and mathematical models. We find that speciation rates estimated from these different studies can be dramatically different: some studies find that new species form quickly and often, while others find that new species form much less frequently. We suggest that instead of being contradictory, differences in speciation rates across different scales can be reconciled by a common model. Under the “ephemeral speciation model”, speciation is very common and very rapid but the new species produced almost never persist. Evolutionary studies should therefore focus on not only the formation but also the persistence of new species.

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.

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.

Congruification: support for time scaling large phylogenetic trees

Summary 1. Approaches for efficient statistical estimation of large phylogenies are now available (Bioinformatics, 2006, 22, 2688), and yet we lack adequate tools for synthesizing information from previous analyses into large timetrees. Here, we present a cross-platform R tool that integrates with tree of life efforts by mapping divergence times from an existing timetree (a ‘reference’) to another uncalibrated phylogeny (a ‘target’) that samples from the same lineage. Leveraging existing methods for rate-smoothing phylograms, this tool enables the rapid generation of very large timetrees where direct estimation of the timing of lineage diversification is either impracticable or impossible. 2. The primary output of the tool is to return divergence times for nodes resolved as concordant between the reference and target. Given the computed set of secondary calibrations, post hoc tree transformation can be accomplished using existing resources that assume either a strict or relaxed evolutionary clock. 3. Our software is provided open source in theGEIGER package (http://cran.r-project.org/package=geiger) and is thoroughly demonstrated in the Supporting Information.

The onion model, a simple neutral model for the evolution of diversity in bacterial biofilms

Bacterial biofilms are particularly resistant to a wide variety of antimicrobial compounds. Their persistence in the face of antibiotic therapies causes significant problems in the treatment of infectious diseases. Seldom have evolutionary processes like genetic drift and mutation been invoked to explain how resistance to antibiotics emerges in biofilms, and we lack a simple and tractable model for the genetic and phenotypic diversification that occurs in bacterial biofilms. Here, we introduce the ‘onion model’, a simple neutral evolutionary model for phenotypic diversification in biofilms. We explore its properties and show that the model produces patterns of diversity that are qualitatively similar to observed patterns of phenotypic diversity in biofilms. We suggest that models like our onion model, which explicitly invoke evolutionary process, are key to understanding biofilm resistance to bactericidal and bacteriostatic agents. Elevated phenotypic variance provides an insurance effect that increases the likelihood that some proportion of the population will be resistant to imposed selective agents and may thus enhance persistence of the biofilm. Accounting for evolutionary change in biofilms will improve our ability to understand and counter diseases that are caused by biofilm persistence.

Inference of Evolutionary Jumps in Large Phylogenies using Lévy Processes

Abstract Although it is now widely accepted that the rate of phenotypic evolution may not necessarily be constant across large phylogenies, the frequency and phylogenetic position of periods of rapid evolution remain unclear. In his highly influential view of evolution, G. G. Simpson supposed that such evolutionary jumps occur when organisms transition into so-called new adaptive zones, for instance after dispersal into a new geographic area, after rapid climatic changes, or following the appearance of an evolutionary novelty. Only recently, large, accurate and well calibrated phylogenies have become available that allow testing this hypothesis directly, yet inferring evolutionary jumps remains computationally very challenging. Here, we develop a computationally highly efficient algorithm to accurately infer the rate and strength of evolutionary jumps as well as their phylogenetic location. Following previous work we model evolutionary jumps as a compound process, but introduce a novel approach to sample jump configurations that does not require matrix inversions and thus naturally scales to large trees. We then make use of this development to infer evolutionary jumps in Anolis lizards and Loriinii parrots where we find strong signal for such jumps at the basis of clades that transitioned into new adaptive zones, just as postulated by Simpson’s hypothesis. [evolutionary jump; Lévy process; phenotypic evolution; punctuated equilibrium; quantitative traits.