Andrew L. Hipp

Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae)

The endemic Hawaiian lobeliads are exceptionally species rich and exhibit striking diversity in habitat, growth form, pollination biology and seed dispersal, but their origins and pattern of diversification remain shrouded in mystery. Up to five independent colonizations have been proposed based on morphological differences among extant taxa. We present a molecular phylogeny showing that the Hawaiian lobeliads are the product of one immigration event; that they are the largest plant clade on any single oceanic island or archipelago; that their ancestor arrived roughly 13 Myr ago; and that this ancestor was most likely woody, wind-dispersed, bird-pollinated, and adapted to open habitats at mid-elevations. Invasion of closed tropical forests is associated with evolution of fleshy fruits. Limited dispersal of such fruits in wet-forest understoreys appears to have accelerated speciation and led to a series of parallel adaptive radiations in Cyanea, with most species restricted to single islands. Consistency of Cyanea diversity across all tall islands except Hawai i suggests that diversification of Cyanea saturates in less than 1.5 Myr. Lobeliad diversity appears to reflect a hierarchical adaptive radiation in habitat, then elevation and flower-tube length, and provides important insights into the pattern and tempo of diversification in a species-rich clade of tropical plants.

Congruence Versus Phylogenetic Accuracy: Revisiting the Incongruence Length Difference Test

Phylogenies inferred from independent data partitions usually differ from one another in topology despite the fact that they are drawn from the same set of organisms (Rodrigo et al., 1993). Some topological differences are due to sampling error or to the use of inappropriate phylogenetic models. These types of topological incongruence do not have their origin in genealogical discordance, i.e., differences between phylogenies underlying the respective data partitions (Baum et al., 1998). Incongruence that is not due to genealogical discordance can often be addressed by modifying the model used in phylogenetic reconstruction (Cunningham, 1997b), and combining data is an appropriate way of dealing with random topological differences that are attributable to sampling error. However, other topological differences, e.g., those arising from lineage sorting (Maddison, 1997; Avise, 2000) and hybridization (Dumolin-Lapegue et al., 1997; Rieseberg, 1997; McKinnon et al., 1999; Avise, 2000), reflect genealogical discordance between the data partitions. Most systematists consider data partitions to be combinable if and only if they are not strongly incongruent with one another (Sytsma, 1990; Bull et al., 1993; Huelsenbeck et al., 1996; Baum et al., 1998; Johnson and Soltis, 1998; Thornton and DeSalle, 2000; Yoder et al., 2001; Barker and Lutzoni, 2002; Buckley et al., 2002). Systematists who follow this prior agreement or conditional combination approach to analyzing multiple data partitions (Bull et al., 1993; Huelsenbeck et al., 1996; Johnson and Soltis, 1998) evaluate incongruence using tests such as the incongruence length difference (ILD) test (Farris et al., 1994, 1995) or other tests of taxonomic congruence (Templeton, 1983; Kishino and Hasegawa, 1989; Larson, 1994; Shimodaira and Hasegawa, 1999) before deciding whether the partitions should be analyzed in combination. Data that exhibit strong incongruence are then analyzed separately or under assumptions that minimize incongruence (Cunningham, 1997b). In their article “Failure of the ILD to determine data combinability for slow loris phylogeny,” Yoder et al. (2001) critiqued the ILD test based on the observation that it will sometimes identify data partitions as incongruent when in fact those partitions combine to produce an accurate estimate of organismal phylogeny. They described the ILD test as a failed test of data combinability, maintaining that the presumed accuracy of trees inferred from combined data indicates the congruence of the data partitions. We have two objections to their argument (2001:421) that “the ILD [should] never be used as a test of data partition combinability.” First, what Yoder et al. described as a flaw in the ILD test as applied to their data, i.e., an apparent inverse relationship between phylogenetic accuracy and data partition congruence as measured by the ILD test, turns out to be an artifact of analysis. There is in fact a bimodal relationship between congruence and accuracy: as either data partition is upweighted, homoplasy in the combined data set is swamped by homoplasy within the upweighted data partition, reducing the significance of the ILD test. At the same time, the topology of the combined analysis shifts to reflect the topology of the upweighted data partition. This phenomenon is predictable and can be accounted for in the analysis (Dowton and Austin, 2002). Second, Yoder et al.’s expectation that ILD test results should predict the phylogenetic accuracy of the combined data analysis is unreasonable. The ILD test is used to evaluate the null hypothesis that characters that make up two or more data partitions are drawn at random from a single population of characters, i.e., a population of characters that reflects a single phylogeny and a single set of evolutionary processes (Farris et al., 1995). Because accuracy of trees derived from a data set depends on many factors other than congruence among data partitions, the ILD test cannot be used to directly address questions related to phylogenetic accuracy. Genealogically discordant data can be combined to yield accurate phylogenies, whereas data that are congruent (both genealogically concordant and homogeneous in underlying evolutionary process) can be combined to yield phylogenies that do not accurately represent organismal history (Cunningham, 1997a). A damaging critique of the ILD test would have to appeal to criteria other than

Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks

Introduced plants tend to experience less herbivory than natives, although herbivore loads vary widely. Herbivores may switch hosts onto an introduced plant for at least two reasons. They may recognize the novel plant as a potential host based on similarity of the plants traits to the traits of one of its native hosts, a similarity that may or may not exhibit phylogenetic signal. Alternatively, herbivores may feed optimally, assessing which introduced plants provide the best nutrition irrespective of similarity to native species. Here, we created a phylogeny of 57 oak (Quercus) taxa, which were grown outside of their ranges in a common botanical garden that contained one abundant native oak (Quercus lobata). We used the phylogeny to estimate the phylogenetic conservatism of herbivory by two feeding guilds of insects (leaf chewers and leaf miners) and 11 plant traits expected to affect herbivore performance. We found high phylogenetic signal in chewing damage but not mining damage and all traits except for leaf maturation time. Introduced oaks that are more closely related to the native oak received more chewing and mining damage than distantly related oaks, and introduced oaks that had greater overall similarity in leaf traits also received higher chewing damage but not mining damage. These results demonstrate that interactions between introduced plants and their herbivores are driven independently by traits that track plant phylogeny and leaf traits that likely affect herbivore performance.

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.

Molecular phylogenetics of the giant genus Croton and tribe Crotoneae (Euphorbiaceae sensu stricto) using ITS and TRNL-TRNF DNA sequence data

Parsimony, likelihood, and Bayesian analyses of nuclear ITS and plastid trnL-F DNA sequence data are presented for the giant genus Croton (Euphorbiaceae s.s.) and related taxa. Sampling comprises 88 taxa, including 78 of the estimated 1223 species and 29 of the 40 sections previously recognized of Croton. It also includes the satellite genus Moacroton and genera formerly placed in tribe Crotoneae. Croton and all sampled segregate genera form a monophyletic group sister to Brasiliocroton, with the exception of Croton sect. Astraea, which is reinstated to the genus Astraea. A small clade including Moacroton, Croton alabamensis, and C. olivaceus is sister to all other Croton species sampled. The remaining Croton species fall into three major clades. One of these is entirely New World, corresponding to sections Cyclostigma, Cascarilla, and Velamea sensu Webster. The second is entirely Old World and is sister to a third, also entirely New World clade, which is composed of at least 13 of Websters sections of Croton. This study establishes a phylogenetic framework for future studies in the hyper-diverse genus Croton, indicates a New World origin for the genus, and will soon be used to evaluate wood anatomical, cytological, and morphological data in the Crotoneae tribe.

A Framework Phylogeny of the American Oak Clade Based on Sequenced RAD Data

Previous phylogenetic studies in oaks (Quercus, Fagaceae) have failed to resolve the backbone topology of the genus with strong support. Here, we utilize next-generation sequencing of restriction-site associated DNA (RAD-Seq) to resolve a framework phylogeny of a predominantly American clade of oaks whose crown age is estimated at 23–33 million years old. Using a recently developed analytical pipeline for RAD-Seq phylogenetics, we created a concatenated matrix of 1.40 E06 aligned nucleotides, constituting 27,727 sequence clusters. RAD-Seq data were readily combined across runs, with no difference in phylogenetic placement between technical replicates, which overlapped by only 43–64% in locus coverage. 17% (4,715) of the loci we analyzed could be mapped with high confidence to one or more expressed sequence tags in NCBI Genbank. A concatenated matrix of the loci that BLAST to at least one EST sequence provides approximately half as many variable or parsimony-informative characters as equal-sized datasets from the non-EST loci. The EST-associated matrix is more complete (fewer missing loci) and has slightly lower homoplasy than non-EST subsampled matrices of the same size, but there is no difference in phylogenetic support or relative attribution of base substitutions to internal versus terminal branches of the phylogeny. We introduce a partitioned RAD visualization method (implemented in the R package RADami; http://cran.r-project.org/web/packages/RADami) to investigate the possibility that suboptimal topologies supported by large numbers of loci—due, for example, to reticulate evolution or lineage sorting—are masked by the globally optimal tree. We find no evidence for strongly-supported alternative topologies in our study, suggesting that the phylogeny we recover is a robust estimate of large-scale phylogenetic patterns in the American oak clade. Our study is one of the first to demonstrate the utility of RAD-Seq data for inferring phylogeny in a 23–33 million year-old clade.

The Evolution of Chromosome Arrangements in Carex (Cyperaceae)

Sedges (Carex: Cyperaceae) exhibit remarkable agmatoploid chromosome series between and within species. This chromosomal diversity is due in large part to the structure of the holocentric chromosomes: fragments that would not be heritable in organisms with monocentric chromosomes have the potential to produce viable gametes in organisms with holocentric chromosomes. The rapid rate of chromosome evolution in the genus and high species diversification rate in the order (Cyperales Hutch., sensu Dahlgren) together suggest that chromosome evolution may play an important role in the evolution of species diversity in Carex. Yet the other genera of the Cyperaceae and their sister group, the Juncaceae, do not show the degree of chromosomal variation found in Carex, despite the fact that diffuse centromeres are a synapomorphy for the entire clade. Moreover, fission and fusion apparently account for the majority of chromosome number changes in Carex, with relatively little duplication of whole chromosomes, whereas polyploidy is relatively important in the other sedge genera. In this paper, we review the cytologic and taxonomic literature on chromosome evolution in Carex and identify unanswered questions and directions for future research. In the end, an integration of biosystematic, cytogenetic, and genomic studies across the Cyperaceae will be needed to address the question of what role chromosome evolution plays in species diversification within Carex and the Cyperaceae as a whole.

Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): a genomic and population genetics approach

The nature and timing of evolution of niche differentiation among closely related species remains an important question in ecology and evolution. The American live oak clade, Virentes, which spans the unglaciated temperate and tropical regions of North America and Mesoamerica, provides an instructive system in which to examine speciation and niche evolution. We generated a fossil‐calibrated phylogeny of Virentes using RADseq data to estimate divergence times and used nuclear microsatellites, chloroplast sequences and an intron region of nitrate reductase (NIA‐i3) to examine genetic diversity within species, rates of gene flow among species and ancestral population size of disjunct sister species. Transitions in functional and morphological traits associated with ecological and climatic niche axes were examined across the phylogeny. We found the Virentes to be monophyletic with three subclades, including a southwest clade, a southeastern US clade and a Central American/Cuban clade. Despite high leaf morphological variation within species and transpecific chloroplast haplotypes, RADseq and nuclear SSR data showed genetic coherence of species. We estimated a crown date for Virentes of 11 Ma and implicated the formation of the Sea of Cortés in a speciation event ~5 Ma. Tree height at maturity, associated with fire tolerance, differs among the sympatric species, while freezing tolerance appears to have diverged repeatedly across the tropical–temperate divide. Sympatric species thus show evidence of ecological niche differentiation but share climatic niches, while allopatric and parapatric species conserve ecological niches, but diverge in climatic niches. The mode of speciation and/or degree of co‐occurrence may thus influence which niche axis plants diverge along.

GLOBAL PATTERNS OF LEAF DEFENSES IN OAK SPECIES

Plant defensive traits drive patterns of herbivory and herbivore diversity among plant species. Over the past 30 years, several prominent hypotheses have predicted the association of plant defenses with particular abiotic environments or geographic regions. We used a strongly supported phylogeny of oaks to test whether defensive traits of 56 oak species are associated with particular components of their climatic niche. Climate predicted both the chemical leaf defenses and the physical leaf defenses of oaks, whether analyzed separately or in combination. Oak leaf defenses were higher at lower latitudes, and this latitudinal gradient could be explained entirely by climate. Using phylogenetic regression methods, we found that plant defenses tended to be greater in oak species that occur in regions with low temperature seasonality, mild winters, and low minimum precipitation, and that plant defenses may track the abiotic environment slowly over macroevolutionary time. The pattern of association we observed between oak leaf traits and abiotic environments was consistent with a combination of a seasonality gradient, which may relate to different herbivore pressures, and the resource availability hypothesis, which posits that herbivores exert greater selection on plants in resource‐limited abiotic environments.

Nonuniform processes of chromosome evolution in sedges (Carex: Cyperaceae).

Abstract Holocentric chromosomes—chromosomes that lack localized centromeres—occur in numerous unrelated clades of insects, flatworms, and angiosperms. Chromosome number changes in such organisms often result from fission and fusion events rather than polyploidy. In this study, I test the hypothesis that chromosome number evolves according to a uniform process in Carex section Ovales (Cyperaceae), the largest New World section of an angiosperm genus renowned for its chromosomal variability and species richness. I evaluate alternative models of chromosome evolution that allow for shifts in both stochastic and deterministic evolutionary processes and that quantify the rate of evolution and heritability/phylogenetic dependence of chromosome number. Estimates of Ornstein–Uhlenbeck model parameters and tree-scaling parameters in a generalized least squares framework demonstrate that (1) chromosome numbers evolve rapidly toward clade-specific stationary distributions that cannot be explained by constant variance (Brownian motion) evolutionary models, (2) chromosome evolution in the section is rapid and exhibits little phylogenetic inertia, and (3) explaining the phylogenetic pattern of chromosome numbers in the section entails inferring a shift in evolutionary dynamics at the root of a derived clade. The finding that chromosome evolution is not a uniform process in sedges provides a novel example of karyotypic orthoselection in an organism with holocentric chromosomes.