Genome-scale data, angiosperm relationships, and "ending incongruence": a cautionary tale in phylogenetics

As systematists grapple with assembling the Tree of Life, recent studies have encouraged a genomic-scale approach, obtaining DNA sequence data for entire nuclear, plastid or mitochondrial genomes for a few exemplar taxa. Some have proclaimed that this comparative genomic strategy heralds the end of incongruence in phylogeny reconstruction. Although we applaud the use of many genes to resolve phylogenetic patterns, there is a significant caveat. In spite of, or even because of, the abundant data per taxon, whole-genome sequencing for a few exemplars can provide completely resolved and strongly supported, but incorrect, evolutionary reconstructions. We provide a conspicuous example that includes Amborella, the putative sister of all other extant angiosperms, highlighting the limits of phylogenetics when whole genomes are used but taxon sampling is poor.     

High‐Throughput Sequencing: A Roadmap Toward Community Ecology

High‐throughput sequencing is becoming increasingly important in microbial ecology, yet it is surprisingly under‐used to generate or test biogeographic hypotheses. In this contribution, we highlight how adding these methods to the ecologist toolbox will allow the detection of new patterns, and will help our understanding of the structure and dynamics of diversity. Starting with a review of ecological questions that can be addressed, we move on to the technical and analytical issues that will benefit from an increased collaboration between different disciplines.     

Charles Girard: Relationships and Representation in Nineteenth Century Systematics

Early nineteenth century systematists sought to describe what they called the Natural System or the Natural Classification. In the nineteenth century, there was no agreement about the basis of observed patterns of similarity between organisms. What did these systematists think they were doing, when they named taxa, proposed relationships between taxa, and arranged taxa into representational schemes? In this paper I explicate Charles Frederic Girard’s (1822–1895) theory and method of systematics. A student of Louis Agassiz, and subsequently (1850–1858) a collaborator with Spencer Baird, Girard claimed that natural classificatory methods do not presuppose either a special creationist or an evolutionary theory of the natural world. The natural system, in Girard’s view, comprises three distinct ways in which organisms can be related to each other. Girard analyzed these relationships, and justified his classificatory methodology, by appeal to his embryological and physiological work. Girard offers an explicit theoretical answer to the question, what characters are evidence for natural classificatory hypotheses? I show that the challenge of simultaneously depicting the three distinct types of relationship led Girard to add a third dimension to his classificatory diagrams.     

Extreme habitats that emerged in the Pleistocene triggered divergence of weedy Youngia (Asteraceae) in Taiwan

Weeds with broad distributions and large morphological variation are challenging for systematists and evolutionarily intriguing because their intensive dispersal would likely prevent local morphological differentiation. Study on weeds will help to understand divergence in plants unlikely to be affected by geographical and ecological barriers. We studied Youngia japonica based on nrDNA and cpDNA sequences. This is a widespread native in Asia and invasive worldwide; nevertheless, three subspecies (japonica, longiflora, and formosana) and an undescribed variant occur in Taiwan. Bayesian and the most parsimonious phylogenies revealed that subspecies longiflora is a different linage and independently arrived in Taiwan during the Pleistocene via land connection to the Asian Continent. Bayesian time estimation suggested that Youngia in Taiwan diverged in the lower Pleistocene or more recently. Extreme habitats that emerged in the Pleistocene, i.e., cold mountain ranges for subspecies formosana and xeric, raised coral reefs for the undescribed Youngia variant probably had triggered the divergence. Components of Youngia in Taiwan are not monophyletic; a coalescent-based test suggested incomplete lineage sorting. Nevertheless, the samples within each taxon share unique morphological features suggesting a common gene pool and each taxon has different dominant ITS and/or cpDNA types; these conditions suggest ongoing process toward monophyly via coalescent processes and support the delimitation of intraspecific taxa.     

Morphological Variations within the Ontogeny of Deinonychus antirrhopus (Theropoda,Dromaeosauridae)

This research resulted from the determination that MCZ 8791 is a specimen of Deinonychus antirrhopus between one and two years of age and that the morphological variations within particular growth stages of this taxon have yet to be described. The primary goal of the research is to identify ontogenetic variations in this taxon. Histological analyses determined that the Deinonychus specimens AMNH 3015 and MOR 1178 were adults. Comparisons are made between MCZ 8791 and these adult specimens. The holotype, YPM 5205, and the other associated specimens of this taxon within the YPM collection are similar in size and morphology to AMNH 3015. Further comparisons were made with the three partial specimens OMNH 50268, MCZ 4371, and MOR 1182. Although these specimens represent only a partial ontogenetic series, a number of morphological variations can be described. One secondary goal of this research is to compare the known pattern of variable, informative, ontogenetic characters in MCZ 8791 to a similar pattern of morphological characters in the sub-adult dromaeosaurid specimen Bambiraptor feinbergorum, AMNH FR: 30556. If the characters that have been determined to represent variable juvenile morphology in the ontogeny of Deinonychus are exhibited in Bambiraptor, this study will begin the process of determining whether a similar, conservative, ontogenetic pattern exists throughout the rest of Dromaeosauridae. If defensible, it may reduce the number of sympatric taxa within this clade. The other secondary goal relates to the forelimb function. The approximate body size, forelimb length, wrist development, and the presence of a more prominent olecranon on the ulna of MCZ 8791 support the hypothesis that juveniles of this taxon possessed some form of flight capability.     

A new species of Hyphoderma (Meruliaceae, Polyporales) and its discrimination from closely related taxa

Thirty-five corticioid collections from the Canary Islands and Azores Archipelago were examined morphologically and subjected to molecular phylogenetic analysis. These specimens, almost all collected on endemic and/or xerophilic vegetation, were similar in morphological and ecological characteristics to Hypochnicium prosopidis from the Sonoran Desert (Arizona, USA) and Hyphoderma amoenum. Thirty-seven new ITS nrDNA sequences from these specimens, including the nomenclatural type of the above-mentioned species, were obtained and aligned with homologous sequences from GenBank. These collections were distributed in two strongly supported monophyletic clades. However, similar patterns of morphological variability shared by specimens included in both clades and their differences with related species suggest that they should be described as a single new species. Therefore Hyphoderma macaronesicum is proposed. Studies will be required to test, in a more robust multilocus genealogical framework, whether these populations constitute two cryptic species or whether they are the same taxon. The position of Hypochnicium prosopidis in the resolved tree and its morphological characters suggest that it should be included in Hyphoderma and the new combination Hyphoderma prosopidis is proposed.     

Computer-Intensive Randomization in Systematics

There has been a sort of cottage industry in the development of randomization routines in systematics beginning with the bootstrap and the jackknife and, in a sense, culminating with various Monte Carlo routines that have been used to assess the performance of phylogenetic methods in limiting circumstances. These methods can be segregated into three basic areas of interest: measures of support such as bootstrap, jackknife, Permutation Tail Probability, T‐PTP, and MoJo; measures of how well independent data are correlated in a phylogenetic framework like PCP for coevolution and Manhattan Stratigraphic Measure (MSM) for stratigraphy; and simulation‐based Monte‐Carlo methods for ascertaining relative performance of optimality criteria or coding methods. Although one approach to assessing cospeciation questions has been the randomization of, for example, hosts and parasite trees, it is well established that in questions that are of a correlative type, the association themselves are what should be permuted. This has been applied to Brooks' parsimony analysis previously and here to the recent reconciled tree approach to these questions. Although it is debatable whether the extrinsic temporal position of a fossil can stand as refutation of intrinsic morphological character‐based cladograms, one can, nonetheless, determine the strength and significance of fit of stratigraphic data to a cladogram. The only method available in this regard that has been shown to not be biased by tree shape is the MSM and modifications of that. Another similar approach that is new is applied to evaluating the historical informativeness of base composition biases. Incongruence length difference tests too are essentially correlative in nature and comparing the behavior of “perceived” partitions to randomly determined partitions of the same size has become the standard for interpreting the relative conflict between differently acquired data. Unlike the foregoing, which make full use of the observed structure of the data, Monte Carlo methods require the input of parameters or of models and in that sense the results tend to be lacking in verisimilitude. Nonetheless, these kinds of questions seem to have been those most widely promulgated in our field. The well‐established theoretical proposition that parsimony has problems with adjacent long‐branches was of course illustrated through such methods, much to the concern and angst of systematists. That likelihood later was shown to perform worse than parsimony when those long branches might repel each other has generated less concern and angst. But then many such circumstances can be divined, like the “short‐branch‐mess” problem wherein likelihood has difficulty placing just a single long branch. Overall, then, in the interpretation of these or any other Monte Carlo issues it will be important to critically examine the structure of the modeled process and the scope of inferences that can be drawn therefrom. Modeling situations that are bound to yield results favorable to only one approach (such as unrealistic even splitting of ancestral populations at unrealistically predictable times in examination of the coding of polymorphic data) should be viewed with great caution. More to the point, since history is singular and not repeatable, the utility of statistical approaches may itself be dubious except in very special circumstances—most of the requirements for stochasticity and independence can never be met.     

What Does Palaeontology Contribute to Systematics in a Molecular World?

Palaeontology provides the only direct record for morphological and genetic change through time and uniquely contributes to systematics in two ways: by providing access to denser taxon sampling than is otherwise possible and by dating divergence times. Claims that ancient DNA has survived millions of years in certain fossils suggested the possibility that palaeontology could contribute directly to molecular systematic studies. Unfortunately, none of the supposed geologically ancient DNA records stands up to detailed scrutiny and fossils therefore contribute primarily through the morphological information they preserve. Denser taxon sampling can improve the accuracy of phylogenetic estimates primarily through allowing better discrimination of homoplasy from homology. This in turn leads to more accurate hypotheses of character transformation. Denser taxon sampling also offers the opportunity for more accurate rooting, since more characters can be polarized by reference to a stem-group taxon than to an extant sister-group taxon. Missing data can be a problem for fossils, but is not crippling. Finally the temporal order of clade appearances in the fossil record can provide ancillary evidence for selecting a working phylogeny from among a number of equally most parsimonious cladograms.     

The Concept of Taxon Invariance in Ecology: Do Diversity Patterns Vary with Changes in Taxonomic Resolution?

Diversity patterns cannot be properly interpreted without a theory providing criteria for their evaluation. We propose a concept to prevent artifictions caused by improper consideration of changes in observed patterns due to variation in taxon delimitation. Most biodiversity patterns concern assemblages of species of given higher taxon (e.g. class). Some patterns seem to be universal, e.g., body size distribution, species-abundance distribution, species-area relationship, or the relationship between diversity and energy availability. However, truly universal patterns should not change when we change taxonomic scope by focusing on subtaxa or when we merge several sister taxa together and analyze patterns in resulting higher taxon. Similarly, some patterns may not change when changing the basic unit of the study e.g., when replacing species by genera or families (or any monophyletic clades), although other patterns may not be invariant against the variation of the basic unit. In fact, there are only two possibilities: biodiversity patterns are either taxon-invariant or they vary systematically with taxonomic resolution, which would indicate some fundamental taxonomic level with interesting implications for biological processes behind those patterns. Here we develop the concept of taxon invariance of diversity patterns and apply it on the abovementioned patterns. We show that simple theoretical considerations markedly constrain the set of possible patterns, as some of them cannot be simultaneously valid for both a taxon and its subtaxa – frequency distributions of abundances cannot be simultaneously lognormal for a given taxon and all its subtaxa, the taxa-area relationship cannot follow a power-law for all levels of taxonomic resolution, and energy availability cannot affect diversity of all taxonomic units in the same way. Analyses of the variation in the form of biodiversity patterns with changing taxonomic resolution thus provide an extremely useful tool for revealing properties of respective patterns, their universality and logical consistency.     

A phylogenetic perspective on habitat shifts and diversity in the North American Enallagma damselflies

Community ecologists are increasingly aware that the regional history of taxon diversification can have an important influence on community structure. Likewise, systematists recognize that ecological context can have an important influence on the processes of speciation and extinction that create patterns of descent. We present a phylogenetic analysis of 33 species of a North American radiation of damselflies (Zygoptera: Coenagrionidae: Enallagma Selys), which have been well studied ecologically, to elucidate the evolutionary mechanisms that have contributed to differences in diversity between larval habitats (lakes with and without fish predators). Analysis of molecular variation in 842 bp of the mitochondrial cytochrome oxidase I and II subunit and of the intervening Leu-tRNA and 37 morphological characters resulted in three well-defined clades that are only partially congruent with previous phylogenetic hypotheses. Molecular and morphological data partitions were significantly incongruent (p < .01). Lack of haplotype monophyly within species and small amounts of sequence divergence (< 1%) between related species in three of the four clades suggest that recent, and parallel, speciation has been an important source of community diversity. Reconstruction of habitat preference over the phylogeny suggests that the greater species diversity in fish-containing lake habitats reflects the recency of shifts into the fishless lake habit, although a difference in speciation or extinction rates between the two habitats is difficult to exclude as an additional mechanism.     

A CLADISTIC TEST OF THE TAXON CYCLE AND TAXON PULSE HYPOTHESES

Abstract— A species' habitat preference is intcrpretablc both as a response to present-day conditions and as a result of evolutionary response to historical conditions. The taxon cycle and taxon pulse have been proposed as hypotheses that allow prediction of patterns of habitat specialization within a lineage. Both are based on common assumptions: (1) habitat specialization is largely irreversible in a lineage, (2) ecological specializations arise in a center of origin, and (3) dispersal events leading to current distributions can be ascertained. Eight taxa of Antillean, Mexican, and Central American Carabidae, for which cladistic hypotheses of relationship have been proposed, are used to test the generality of the taxon cycle and pulse. The patterns of habitat utilization predicted by the taxon cycle and taxon pulse hypotheses are tested by comparing cladistic transformations of habitat preference to randomly generated patterns of data generated under a null hypothesis. Evolutionary changes in habitat are interpreted using Camin-Sokal coding, which assumes irreversible habitat shifts and a predetermined ecological ground state (assumptions of the taxon cycle and taxon pulse). An observed pattern is considered to demonstrate the taxon cycle or pulse when it results in an explanation of the habitat shifts that is more parsimonious than 95 % of the randomly generated patterns. Of the eight carabid groups, only one exhibits a statistically significant pattern supporting the taxon cycle and pulse. The failure of the taxon cycle and pulse as generally predictive hypotheses may be due to historical changes in climate that permit episodes of range expansion for species previously restricted to small ranges, and habitat shifts and specialization that do not progress in a linear transformation series. Habitat shifts are also analyzed using Farris optimization, resulting in the most parsimonious transformation series of habitats, subject to a predefined ordering of habitats, while allowing reversals. Significance of an observed pattern of habitat shifts under Farris optimization implies habitat constancy relative to cladogenesis, and step-wise changes in habitat preference. Two of the eight groups exhibit significant patterns of habitat utilization under Farris optimization, indicating that vicariance of areas of like habitat has been the predominant factor generating species diversity in these groups. The other groups do not exhibit habitat constancy, suggesting rapid changes in habitat preference relative to speciation.     

Systematics and biogeography of the Andean genusEriocnemis (Aves: Trochilidae)

Summary With 11 currently recognised species, the genusEriocnemis (Reichenbach, 1849) is one of the most diversified Andean trochilid groups occupying mainly open montane habitats such as the edges of cloud forest or páramos. On the basis of distributional and morphological patterns, this study highlights the geographical variation and biogeography of the taxon. Characteristics common to all these species are the greenish dorsal plumage, the conspicuous and mostly whitish tibial tufts, and a fairly pronounced tail bifurcation. With the help of plumage synapomorphies for a cladistic analysis (PAUP*), several species groups or superspecies can be distinguished: theE. vestitus group (incl.E. vestitus, E. godini, E. nigrivestis), theE. luciani group (incl.E. luciani, E. cupreoventris, E. sapphiropygia), and theE. alinae group (incl.E. alinae, E. mirabilis).E. glaucopoides, E. mosquera, andE. derbyi differ quite widely in morphology and ecological requirements from the other species. Three new subspecies are described,E. vestitus arcosi from southern Ecuador and northern Peru, andE. luciani baptistae from central and southern Ecuador. A previously overlooked specimen ofE. luciani from the Andes of Mérida represents the first species record for Venezuela, about 1100 km northeast of the main population range, and should be recognised taxonomically asE. luciani meridae, subsp. nov., on the basis of its unique plumage morphology and geographical separation. Additionally, the unique type ofE. ventralis (Salvin, 1891) is probably of hybrid origin (E. vestitus × cupreoventris). The genus may have evolved in the northern Andes, subsequently spreading southward and invading the central Andes. Its recent range and phylogenetic patterns indicate vicariance events as the major speciation factor inEriocnemis.In memoriam Dr. Luis F. Baptista (1941–2000)     

Rapid cladogenesis in marine fishes revisited

Lineages that underwent rapid cladogenesis are attractive systems for the study of mechanisms underlying taxonomic, ecological, morphological, and behavioral diversification. Recently developed statistical methods provide insights into historical patterns of diversity and allow distinguishing bursts of cladogenesis from stochastic background rates in the presence of confounding factors such as extinction and incomplete taxon sampling. Here, we compare the dynamics of speciation in several marine fish lineages some of which were previously proposed to have undergone significant changes of cladogenesis through time. We tested for evidence of episodes of rapid cladogenesis using the constant rate and Monte Carlo constant rate tests that are robust to incomplete taxon sampling. These tests employ the statistic gamma to measure the relative position of internal node in a chronogram. For the first time, we conducted a comparative analysis to address the behavior of the statistic under different chronogram-constructing methods (Langley-Fitch, nonparametric rate smoothing, and penalized likelihood). Although estimates of gamma sometimes differ widely among methods, acceptance or rejection of the constant rate model within a particular clade appears to be robust to the choice of method. Bursts of cladogenesis were detected in 14 of 34 studied datasets. Some of these were previously proposed to represent marine fish "radiations," whereas others are identified anew. Our results indicate that the wider application of tree shape methods that are able to detect significantly elevated rates of speciation is useful to more precisely define clades that underwent episodes of rapid cladogenesis in marine fish clades. Contrasting the patterns of phylogenetic diversification in marine fish lineages may facilitate the identification of common evolutionary trajectories versus idiosyncrasies, and ultimately help towards a better understanding of the factors and processes underlying speciation in the marine realm.     

Ecological niche modelling as an exploratory tool for identifying species limits: an example based on Mexican muroid rodents

Niche conservatism theory suggests that recently diverged sister species share the same ecological niche. However, if the ecological niche evolves as part of the speciation process, the ecological pattern could be useful for recognizing cryptic species. In a broad sense systematists agree that the niche characters could be used for species differentiation. However, to date such characters have been ignored. We used the genetic algorithm for rule‐set production for modelling the ecological niche as a means of inferring ecological divergence in allopatric populations of muroid rodents for which taxonomic identity is uncertain. Our results show that niche differentiation is significant in most of the identified phylogroups. The differentiation is likely associated with natural evolutionary units, which can be identified by applying species concepts based on phylogenetic and ecological patterns (e.g. phylogenetic, cohesive, evolutionary). Even so, the role of the niche partition within phylogenetic reconstruction may be a limited one.     

Testing Hypotheses of Evolutionary Relationships Among Parasites: The Digeneans of Crocodilians

Parasite systematists may question whether or not all the parasitesof a given host taxon share a common evolutionary history, especiallyone which also includes the host taxon. This study presentsa method for testing hypotheses of such faunal coevolution usingcrocodilians and their digeneans as a model host-parasite system.First, phylogenetic analysis, using numerical methods when largedata bases require such handling, produces estimates of genealogicalrelationships among members of various taxa represented. Theestimates, in the form of branching diagrams (cladograms), caneach be compared with host genealogy and with geographic genealogyfor the areas in which the parasites occur. Congruence of suchpatterns suggests a common evolutionary history and corroboratesan hypothesis of faunal coevolution; incongruence suggests aninvasive or colonizing fauna and falsifies an hypothesis offaunal coevolution. The digeneans of crocodilians apparentlyhave coevolved as a faunal unit with their host group, at leastsince the end of the Mesozoic.     

Multivariate analyses in microbial ecology

Environmental microbiology is undergoing a dramatic revolution due to the increasing accumulation of biological information and contextual environmental parameters. This will not only enable a better identification of diversity patterns, but will also shed more light on the associated environmental conditions, spatial locations, and seasonal fluctuations, which could explain such patterns. Complex ecological questions may now be addressed using multivariate statistical analyses, which represent a vast potential of techniques that are still underexploited. Here, well-established exploratory and hypothesis-driven approaches are reviewed, so as to foster their addition to the microbial ecologist toolbox. Because such tools aim at reducing data set complexity, at identifying major patterns and putative causal factors, they will certainly find many applications in microbial ecology.     

Investigating species–environment relationships at multiple scales: Differentiating between intrinsic scale and the modifiable areal unit problem

In ecology, multi-scale analyses are commonly performed to identify the scale at which a species interacts with its environment (intrinsic scale). This is typically carried out using multi-scale species–environment models that compare the relationship between ecological attributes (e.g., species diversity) measured with point data to environmental data (e.g. vegetation cover) for the surrounding area within buffers of multiple sizes. The intrinsic scale is identified as the buffer size at which the highest correlation between environmental and ecological variables occurs. We present the first investigation of how the spatial resolution of remote sensing environmental data can influence the identification of the intrinsic scale using multi-scale species–environment models. Using the virtual ecologist approach we tested this influence using vegetation cover spatial data and a simulated species–environment relationship derived from the same spatial data. By using a simulation model there was a known truth to use as a benchmark to measure accuracy. Our findings indicate that by varying the spatial resolution of the environmental data, the intrinsic scale may be incorrectly identified. In some cases, the errors in the intrinsic scale identified were close to the maximum value possible that could be measured by this experiment. Consequently, multi-scale ecological analyses may not be suitable for distinguishing scale patterns caused by the relationship between an organism and its environment from scale patterns caused by the effect of changing spatial resolution: a phenomenon referred to as the modifiable areal unit problem (MAUP). Thus, observed scale-dependent ecological patterns may be an artefact of the observation of ecological data, not the ecological phenomenon. This study concludes with some suggestions for future work to quantify the effect of the MAUP on multi-scale studies and develop generalisations that can be used to assess when multi-scale analyses have the potential to produce spurious results.     

Detecting the structural and functional impacts of fine sediment on stream invertebrates

Fine sediment is one of the major sources of stream physical and ecological impairment worldwide. We assessed the ecological effects of fine sediment in an otherwise undisturbed catchment (the Isábena, NE Spain). Using data from sites across the catchment we describe the spatial variability and nestedness of invertebrate assemblages and evaluate the effectiveness of compositional (taxon-based) and functional (trait-based) metrics for detecting sediment impacts on these assemblages.Invertebrate assemblages were relatively taxon poor and had low densities in those locations with high fine sediment content. Assemblages showed significantly nested patterns, with those in sediment-rich locations consisting of a subset of those in locations with little fine sediment. A number of biological traits appeared to promote this nestedness, particularly those conferring resistance and resilience to fine sediment (polivoltinism, short live cycles and small body sizes).Generalised Additive Models indicated that most metrics were able to detect ecological responses to sedimentation. Some taxon-based metrics (%EPT and evenness) performed less well, with values showing only a weak relationship with fine sediment. Results are consistent with previous studies which have highlighted the limitations of taxon-based metrics and suggest that indices of functional diversity are capable of detecting sediment related impairment.Overall, the study suggests that fine sediment in the Isábena was selecting for specific life-history traits, and that this selection resulted in clear differences in assemblage structure across the catchment. The use of biological traits in studies of sediment related disturbance may help identify extinction-prone species (e.g. those with univoltine and/or long life-cycles), while trait-based monitoring and assessment metrics, because they reflect the ecological mechanisms underlying observed patterns, should prove useful to help guide management in catchments subjected to excessive fine sediment. More broadly, the study indicates that nestedness in assemblage structure can be driven by local habitat changes, and not only by large scale biogeographical processes.