Deconstructing age estimates for angiosperms.

Estimates of the age of angiosperms from molecular phylogenies vary considerably. As in all estimates of evolutionary timescales from phylogenies, generating these estimates requires assumptions about the rate that molecular sequences are evolving (using clock models) and the time duration of the branches in a phylogeny (using fossil calibrations and branching processes). Often, it is difficult to demonstrate that these assumptions reflect current knowledge of molecular evolution or the fossil record. In this study we re-estimate the age of angiosperms using a minimal set of assumptions, therefore avoiding many of the assumptions inherent to other methods. The age estimates we generate are similar for each of the four datasets analysed, ranging from 130 to 400 Ma, but are far less precise than in previous studies. We demonstrate that this reduction in precision results from making less stringent assumptions about both rate and time, and that the analysed molecular dataset has very little effect on age estimates.

Species as a Heuristic: Reconciling Theory and Practice.

Species are crucial to most branches of biological research, yet remain controversial in terms of definition, delimitation, and reality. The difficulty of resolving the "species problem" stems from the tension between their theoretical concept as groups of evolving and highly variable organisms and the practical need for a stable and comparable unit of biology. Here, we suggest that treating species as a heuristic can be consistent with a theoretical definition of what species are and with the practical means by which they are identified and delimited. Specifically, we suggest that theoretically species are heuristic since they comprise clusters of closely related individuals responding in a similar manner to comparable sets of evolutionary and ecological forces, whilst they are practically heuristic because they are identifiable by the congruence of contingent properties indicative of those forces. This reconciliation of the theoretical basis of species with their practical applications in biological research allows for a loose but relatively consistent definition of species based on the strategic analysis and integration of genotypic, phenotypic, and ecotypic data. [Cohesion; heuristic; homeostasis; lineage; species problem.].

Discovery and characterization of sweetpotato's closest tetraploid relative.

The origin of sweetpotato, a hexaploid species, is poorly understood, partly because the identity of its tetraploid progenitor remains unknown. In this study, we identify, describe and characterize a new species of Ipomoea that is sweetpotato's closest tetraploid relative known to date and probably a direct descendant of its tetraploid progenitor. We integrate morphological, phylogenetic, and genomic analyses of herbarium and germplasm accessions of the hexaploid sweetpotato, its closest known diploid relative Ipomoea trifida, and various tetraploid plants closely related to them from across the American continent. We identify wild autotetraploid plants from Ecuador that are morphologically distinct from Ipomoea batatas and I. trifida, but monophyletic and sister to I. batatas in phylogenetic analysis of nuclear data. We describe this new species as Ipomoea aequatoriensis T. Wells & P. Muñoz sp. nov., distinguish it from hybrid tetraploid material collected in Mexico; and show that it likely played a direct role in the origin of sweetpotato's hexaploid genome. This discovery transforms our understanding of sweetpotato's origin.

Uncertainty in Divergence Time Estimation.

Understanding and representing uncertainty is crucial in academic research because it enables studies to build on the conclusions of previous studies, leading to robust advances in a particular field. Here, we evaluate the nature of uncertainty and the manner by which it is represented in divergence time estimation, a field that is fundamental to many aspects of macroevolutionary research, and where there is evidence that uncertainty has been seriously underestimated. We address this issue in the context of methods used in divergence time estimation, and with respect to the manner by which time-calibrated phylogenies are interpreted. With respect to methods, we discuss how the assumptions underlying different methods may not adequately reflect uncertainty about molecular evolution, the fossil record, or diversification rates. Therefore, divergence time estimates may not adequately reflect uncertainty and may be directly contradicted by subsequent findings. For the interpretation of time-calibrated phylogenies, we discuss how the use of time-calibrated phylogenies for reconstructing general evolutionary timescales leads to inferences about macroevolution that are highly sensitive to methodological limitations in how uncertainty is accounted for. By contrast, we discuss how the use of time-calibrated phylogenies to test specific hypotheses leads to inferences about macroevolution that are less sensitive to methodological limitations. Given that many biologists wish to use time-calibrated phylogenies to reconstruct general evolutionary timescales, we conclude that the development of methods of divergence time estimation that adequately account for uncertainty is necessary. [Divergence time estimation; macroevolution; uncertainty.].

The Implications of Interrelated Assumptions on Estimates of Divergence Times and Rates of Diversification.

Phylogenies are increasingly being used as a basis to provide insight into macroevolutionary history. Here, we use simulation experiments and empirical analyses to evaluate methods that use phylogenies as a basis to make estimates of divergence times and rates of diversification. This is the first study to present a comprehensive assessment of the key variables that underpin analyses in this field-including substitution rates, speciation rates, and extinction, plus character sampling and taxon sampling. We show that in unrealistically simplistic cases (where substitution rates and speciation rates are constant, and where there is no extinction), increased character and taxon sampling lead to more accurate and precise parameter estimates. By contrast, in more complex but realistic cases (where substitution rates, speciation rates, and extinction rates vary), gains in accuracy and precision from increased character and taxon sampling are far more limited. The lack of accuracy and precision even occurs when using methods that are designed to account for more complex cases, such as relaxed clocks, fossil calibrations, and models that allow speciation rates and extinction rates to vary. The problem also persists when analyzing genomic scale data sets. These results suggest two interrelated problems that occur when the processes that generated the data are more complex. First, methodological assumptions are more likely to be violated. Second, limitations in the information content of the data become more important.[Divergence time estimation; diversification rates; macroevolution; phylogeny.].

Insights from Empirical Analyses and Simulations on Using Multiple Fossil Calibrations with Relaxed Clocks to Estimate Divergence Times.

Relaxed clock methods account for among-branch-rate-variation when estimating divergence times by inferring different rates for individual branches. In order to infer different rates for individual branches, important assumptions are required. This is because molecular sequence data do not provide direct information about rates but instead provide direct information about the total number of substitutions along any branch, which is a product of the rate and time for that branch. Often, the assumptions required for estimating rates for individual branches depend heavily on the implementation of multiple fossil calibrations in a single phylogeny. Here, we show that the basis of these assumptions is often critically undermined. First, we highlight that the temporal distribution of the fossil record often violates key assumptions of methods that use multiple fossil calibrations with relaxed clocks. With respect to "node calibration" methods, this conclusion is based on our inference that different fossil calibrations are unlikely to reflect the relative ages of different clades. With respect to the fossilized birth-death process, this conclusion is based on our inference that the fossil recovery rate is often highly heterogeneous. We then demonstrate that methods of divergence time estimation that use multiple fossil calibrations are highly sensitive to assumptions about the fossil record and among-branch-rate-variation. Given the problems associated with these assumptions, our results highlight that using multiple fossil calibrations with relaxed clocks often does little to improve the accuracy of divergence time estimates.

The Implications of Lineage-Specific Rates for Divergence Time Estimation.

Rate variation adds considerable complexity to divergence time estimation in molecular phylogenies. Here, we evaluate the impact of lineage-specific rates-which we define as among-branch-rate-variation that acts consistently across the entire genome. We compare its impact to residual rates-defined as among-branch-rate-variation that shows a different pattern of rate variation at each sampled locus, and gene-specific rates-defined as variation in the average rate across all branches at each sampled locus. We show that lineage-specific rates lead to erroneous divergence time estimates, regardless of how many loci are sampled. Further, we show that stronger lineage-specific rates lead to increasing error. This contrasts to residual rates and gene-specific rates, where sampling more loci significantly reduces error. If divergence times are inferred in a Bayesian framework, we highlight that error caused by lineage-specific rates significantly reduces the probability that the 95% highest posterior density includes the correct value, and leads to sensitivity to the prior. Use of a more complex rate prior-which has recently been proposed to model rate variation more accurately-does not affect these conclusions. Finally, we show that the scale of lineage-specific rates used in our simulation experiments is comparable to that of an empirical data set for the angiosperm genus Ipomoea. Taken together, our findings demonstrate that lineage-specific rates cause error in divergence time estimates, and that this error is not overcome by analyzing genomic scale multilocus data sets. [Divergence time estimation; error; rate variation.].

The temporal dynamics of evolutionary diversification in Ipomoea.

Molecular phylogenies are used as a basis for making inferences about macroevolutionary history. However, a robust phylogeny does not contain the information that is necessary to make many of these inferences. Complex methodologies that incorporate important assumptions about the nature of evolutionary history are therefore required. Here, we explore the implications of these assumptions for making inferences about the macroevolutionary history of Ipomoea - a large pantropical genus of flowering plants that contains the sweet potato (Ipomoea batatas), a crop of global economic importance. We focus on assumptions that underlie inferences of divergence times, and diversification parameters (speciation rates, extinction rates, and net diversification rates). These are among the most fundamental variables in macroevolutionary research. We use a series of novel approaches to explore the implications of these assumptions for inferring the age of Ipomoea, the ages of major clades within Ipomoea, whether there are significant differences in diversification parameters among clades within Ipomoea, and whether the storage root of I. batatas evolved in pre-human times. We show that inferring an age estimate for Ipomoea and major clades within Ipomoea is highly problematic. Inferred divergence times are sensitive to uncertain fossil calibrations and differing assumptions about among-branch-substitution-rate-variation. Despite this uncertainty, we are able to make robust inferences about patterns of variation in diversification parameters within Ipomoea, and that the storage root of I. batatas evolved in pre-human times. Taken together, this study presents novel and generalizable insights into the implications of methodological assumptions for making inferences about macroevolutionary history. Further, by presenting novel findings relating to the temporal dynamics of evolution in Ipomoea, as well as more specifically to I. batatas, this study makes a valuable contribution to our understanding of tropical plant evolution, and the evolutionary context in which economically important crops evolve.

How the temperate world was colonised by bindweeds: biogeography of the Convolvuleae (Convolvulaceae).

BACKGROUND: At a global scale, the temperate zone is highly fragmented both between and within hemispheres. This paper aims to investigate how the world's disjunct temperate zones have been colonised by the pan-temperate plant group Convolvuleae, sampling 148 of the c. 225 known species. We specifically determine the number and timing of amphitropical and transoceanic disjunctions, investigate the extent to which disjunctions in Convolvuleae are spatio-temporally congruent with those in other temperate plant groups and determine the impact of long-distance dispersal events on diversification rates. RESULTS: Eight major disjunctions are observed in Convolvuleae: two Northern Hemisphere, two Southern Hemisphere and four amphitropical. Diversity in the Southern Hemisphere is largely the result of a single colonisation of Africa 3.1-6.4 Ma, and subsequent dispersals from Africa to both Australasia and South America. Speciation rates within this monophyletic, largely Southern Hemisphere group (1.38 species Myr(-1)) are found to be over twice those of the tribe as a whole (0.64 species Myr(-1)). Increased speciation rates are also observed in Calystegia (1.65 species Myr(-1)). CONCLUSIONS: The Convolvuleae has colonised every continent of the world with a temperate biome in c. 18 Myr and eight major range disjunctions underlie this broad distribution. In keeping with other temperate lineages exhibiting disjunct distributions, long-distance dispersal is inferred as the main process explaining the patterns observed although for one American-Eurasian disjunction we cannot exclude vicariance. The colonisation of the temperate zones of the three southern continents within the last c. 4 Myr is likely to have stimulated high rates of diversification recovered in this group, with lineage accumulation rates comparable to those reported for adaptive radiations.

Circumstances in which parsimony but not compatibility will be provably misleading.

Phylogenetic methods typically rely on an appropriate model of how data evolved in order to infer an accurate phylogenetic tree. For molecular data, standard statistical methods have provided an effective strategy for extracting phylogenetic information from aligned sequence data when each site (character) is subject to a common process. However, for other types of data (e.g., morphological data), characters can be too ambiguous, homoplastic, or saturated to develop models that are effective at capturing the underlying process of change. To address this, we examine the properties of a classic but neglected method for inferring splits in an underlying tree, namely, maximum compatibility. By adopting a simple and extreme model in which each character either fits perfectly on some tree, or is entirely random (but it is not known which class any character belongs to) we are able to derive exact and explicit formulae regarding the performance of maximum compatibility. We show that this method is able to identify a set of non-trivial homoplasy-free characters, when the number [Formula: see text] of taxa is large, even when the number of random characters is large. In contrast, we show that a method that makes more uniform use of all the data-maximum parsimony-can provably estimate trees in which none of the original homoplasy-free characters support splits.

Cardamine hirsuta: a versatile genetic system for comparative studies.

A major goal in biology is to identify the genetic basis for phenotypic diversity. This goal underpins research in areas as diverse as evolutionary biology, plant breeding and human genetics. A limitation for this research is no longer the availability of sequence information but the development of functional genetic tools to understand the link between changes in sequence and phenotype. Here we describe Cardamine hirsuta, a close relative of the reference plant Arabidopsis thaliana, as an experimental system in which genetic and transgenic approaches can be deployed effectively for comparative studies. We present high-resolution genetic and cytogenetic maps for C. hirsuta and show that the genome structure of C. hirsuta closely resembles the eight chromosomes of the ancestral crucifer karyotype and provides a good reference point for comparative genome studies across the Brassicaceae. We compared morphological and physiological traits between C. hirsuta and A. thaliana and analysed natural variation in stamen number in which lateral stamen loss is a species characteristic of C. hirsuta. We constructed a set of recombinant inbred lines and detected eight quantitative trait loci that can explain stamen number variation in this population. We found clear phylogeographic structure to the genetic variation in C. hirsuta, thus providing a context within which to address questions about evolutionary changes that link genotype with phenotype and the environment.

The corona of the daffodil Narcissus bulbocodium shares stamen-like identity and is distinct from the orthodox floral whorls.

The structural homology of the daffodil corona has remained a source of debate throughout the history of botany. Over the years it has been separately referred to as a modified petal stipule, stamen and tepal. Here we provide insights from anatomy and molecular studies to clarify the early developmental stages and position of corona initiation in Narcissus bulbocodium. We demonstrate that the corona initiates as six separate anlagen from hypanthial tissue between the stamens and perianth. Scanning electron microscope images and serial sections demonstrate that corona initiation occurs late in development, after the other floral whorls are fully developed. To define more precisely the identity of the floral structures, daffodil orthologues of the ABC floral organ identity genes were isolated and expression patterns were examined in perianth, stamens, carpel, hypanthial tube and corona tissue. Coupled with in situ hybridisation experiments, these analyses showed that the expression pattern of the C-class gene NbAGAMOUS in the corona is more similar to that of the stamens than that of the tepals. In combination, our results demonstrate that the corona of the daffodil N. bulbocodium exhibits stamen-like identity, develops independently from the orthodox floral whorls and is best interpreted as a late elaboration of the region between the petals and stamens associated with epigyny and the hypanthium.

Author inflation masks global capacity for species discovery in flowering plants.

Species discovery is a fundamental first step for all of biodiversity science. Recent research has claimed that the increasing number of authors associated with the description of new species represents an expanding workforce discovering the remaining new species from an ever-diminishing pool. Here, we present a comprehensive dataset from The International Plant Names Index (IPNI) of new species of flowering plant published between 1970 and 2011. We show that, on average, 1855 new species have been described annually since 1970. We show that compared to other scientific disciplines the increased number of authors on taxonomic papers is relatively small and may reflect changes in scientific practice rather than an increase in taxonomic capacity. These data, alongside published results demonstrating a lag period of 35 yr between a specimen being collected and published as a new species, strongly suggest that the global taxonomic capacity to describe new species of flowering plant is stagnant at a time of unprecedented concern for conservation and extinction.

Herbaria are a major frontier for species discovery.

Despite the importance of species discovery, the processes including collecting, recognizing, and describing new species are poorly understood. Data are presented for flowering plants, measuring quantitatively the lag between the date a specimen of a new species was collected for the first time and when it was subsequently described and published. The data from our sample of new species published between 1970 and 2010 show that only 16% were described within five years of being collected for the first time. The description of the remaining 84% involved much older specimens, with nearly one-quarter of new species descriptions involving specimens >50 y old. Extrapolation of these results suggest that, of the estimated 70,000 species still to be described, more than half already have been collected and are stored in herbaria. Effort, funding, and research focus should, therefore, be directed as much to examining extant herbarium material as collecting new material in the field.

Big hitting collectors make massive and disproportionate contribution to the discovery of plant species.

Discovering biological diversity is a fundamental goal--made urgent by the alarmingly high rate of extinction. We have compiled information from more than 100,000 type specimens to quantify the role of collectors in the discovery of plant diversity. Our results show that more than half of all type specimens were collected by less than 2 per cent of collectors. This highly skewed pattern has persisted through time. We demonstrate that a number of attributes are associated with prolific plant collectors: a long career with increasing productivity and experience in several countries and plant families. These results imply that funding a small number of expert plant collectors in the right geographical locations should be an important element in any effective strategy to find undiscovered plant species and complete the inventory of the world flora.

Deep homology: a view from systematics.

Over the past decade, it has been discovered that disparate aspects of morphology - often of distantly related groups of organisms - are regulated by the same genetic regulatory mechanisms. Those discoveries provide a new perspective on morphological evolutionary change. A conceptual framework for exploring these research findings is termed 'deep homology'. A comparative framework for morphological relations of homology is provided that distinguishes analogy, homoplasy, plesiomorphy and synapomorphy. Four examples - three from plants and one from animals - demonstrate that homologous developmental mechanisms can regulate a range of morphological relations including analogy, homoplasy and examples of uncertain homology. Deep homology is part of a much wider range of phenomena in which biological (genes, regulatory mechanisms, morphological traits) and phylogenetic levels of homology can both be disassociated. Therefore, to understand homology, precise, comparative, independent statements of both biological and phylogenetic levels of homology are necessary.

exTREEmaTIME: a method for incorporating uncertainty into divergence time estimates.

We present a method of divergence time estimation (exTREEmaTIME) that aims to effectively account for uncertainty in divergence time estimates. The method requires a minimal set of assumptions, and, based on these assumptions, estimates the oldest possible divergence times and youngest possible divergence times that are consistent with the assumptions. We use a series of simulations and empirical analyses to illustrate that exTREEmaTIME is effective at representing uncertainty. We then describe how exTREEmaTIME can act as a basis to determine the implications of the more stringent assumptions that are incorporated into other methods of divergence time estimation that produce more precise estimates. This is critically important given that many of the assumptions that are incorporated into these methods are highly complex, difficult to justify biologically, and as such can lead to estimates that are highly inaccurate. This article has an associated First Person interview with the first author of the paper.

Heuristics, species, and the analysis of systematic data.

Disagreements over how to define species potentially render them incomparable, yet biologists routinely count and compare species. This 'species problem' persists despite the wealth of data and methods available to contemporary systematists. A heuristic approach to species provides a consistent yet flexible means of selecting, assessing, and integrating different biological data.

What is parallelism?

Although parallel and convergent evolution are discussed extensively in technical articles and textbooks, their meaning can be overlapping, imprecise, and contradictory. The meaning of parallel evolution in much of the evolutionary literature grapples with two separate hypotheses in relation to phenotype and genotype, but often these two hypotheses have been inferred from only one hypothesis, and a number of subsidiary but problematic criteria, in relation to the phenotype. However, examples of parallel evolution of genetic traits that underpin or are at least associated with convergent phenotypes are now emerging. Four criteria for distinguishing parallelism from convergence are reviewed. All are found to be incompatible with any single proposition of homoplasy. Therefore, all homoplasy is equivalent to a broad view of convergence. Based on this concept, all phenotypic homoplasy can be described as convergence and all genotypic homoplasy as parallelism, which can be viewed as the equivalent concept of convergence for molecular data. Parallel changes of molecular traits may or may not be associated with convergent phenotypes but if so describe homoplasy at two biological levels-genotype and phenotype. Parallelism is not an alternative to convergence, but rather it entails homoplastic genetics that can be associated with and potentially explain, at the molecular level, how convergent phenotypes evolve.

Independent recruitment of a conserved developmental mechanism during leaf evolution.

Vascular plants evolved in the Middle to Late Silurian period, about 420 million years ago. The fossil record indicates that these primitive plants had branched stems with sporangia but no leaves. Leaf-like lateral outgrowths subsequently evolved on at least two independent occasions. In extant plants, these events are represented by microphyllous leaves in lycophytes (clubmosses, spikemosses and quillworts) and megaphyllous leaves in euphyllophytes (ferns, gymnosperms and angiosperms). Our current understanding of how leaves develop is restricted to processes that operate during megaphyll formation. Because microphylls and megaphylls evolved independently, different mechanisms might be required for leaf formation. Here we show that this is not so. Gene expression data from a microphyllous lycophyte, phylogenetic analyses, and a cross-species complementation experiment all show that a common developmental mechanism can underpin both microphyll and megaphyll formation. We propose that this mechanism might have operated originally in the context of primitive plant apices to facilitate bifurcation. Recruitment of this pathway to form leaves occurred independently and in parallel in different plant lineages.