A preliminary phylogenetic study of late Palaeozoic spiriferoid brachiopods using cladistic and Bayesian approaches

The brachiopod Superfamily Spiriferoidea diversified greatly and was widely distributed in the late Palaeozoic (Carboniferous–Permian), and yet its phylogeny has been seldom investigated with analytical methods. This is reflected in the current flux of very different classification schemes for this superfamily. This paper provides the first attempt to investigate the phylogenetic relationships of spiriferoid brachiopods through both cladistic and Bayesian analyses involving 24 discrete and continuous characters. The continuous characters, from morphometric data, have been separately discretized using the gap weighting method, and the ‘as such’ option in TNT. Our results highlight the potential significance of continuous characters in reconstructing and elucidating phylogenies, as much as qualitative characters. Building on the outcomes of the analyses, we also briefly evaluate existing classification schemes of Spiriferoidea. We found that none of the existing classifications fully reflect the phylogeny properly; major families within the superfamily, such as Spiriferidae, Choristitidae, and Trigonotretidae, turned out to be polyphyletic. Although this study is considered preliminary, due to the selection of and restriction to certain taxa, combined with the use of a relatively small number of characters, it nevertheless demonstrates that potentially the true phylogenetic relationships of spiriferoid taxa sharply contrast with any of the existing classification schemes. This highlights the need to develop an alternative scheme that takes into account a more comprehensive range of phylogenetic variables.     

THE HOLY GRAIL OF THE PERFECT CHARACTER: THE CLADISTIC TREATMENT OF MORPHOMETRIC DATA

Abstract— Data scored for cladistic analyses may be quantitative or qualitative, continuous or discrete, and show overlapping or non-overlapping values between taxa. Quantitative and qualitative are modes of expression of data, while continuous or discrete refer to properties of the set of numbers that express the data; both these pairs of terms have been confused with overlapping and non-overlapping. The degree of overlap of values between taxa is often used to filter characters in cladistic analyses: if a minimum amount of overlap is exceeded, or a minimum amount of disjunction not reached, characters are rejected as "not cladistic". However, this rests on a confusion between features of taxa and features of individual organisms (attributes). Cladistic characters are features of taxa, and comprise frequency distributions of attribute values over individuals of a taxon. Cladistic characters logically cannot overlap, although taxa may have overlapping attribute values. Thus, a priori rejection of characters that have overlapping attribute values is non-sensical. Such data may still be rejected from consideration for cladistic analysis if it could be demonstrated that they contain little recoverable phylogenetic signal. Few published analyses have empirically tested this. An analysis of overlapping morphometric data from three series of Banksia suggests that, at least in these cases, they map phylogeny almost as accurately as more conventional, qualitative morphological data. While more such tests are required, morphometric data should not be rejected a priori from cladistic analyses.     

Morphometric variation in the hominoid orbital aperture: a case study with implications for the use of variable characters in Miocene catarrhine systematics

Variable characters are ubiquitous in hominoid systematics and present a number of unique problems for phylogenetic analyses that include extinct taxa. As yet, however, few studies have quantified ranges of variation in complex morphometric characters within extant taxa and then used those data to assess the consistency with which discrete character states can be applied to poorly represented fossil species. In this study, ranges of intrageneric morphometric variation in the shape of the hominoid orbital aperture are estimated using exact randomization of average pairwise taxonomic distances (ATDs) derived from size-adjusted centroid, height-width, and elliptic Fourier (EF) variables. Using both centroid and height-width variables, 19 of the 21 possible ATDs between individuals representing seven extinct catarrhine taxa (Aegyptopithecus, Afropithecus, Ankarapithecus, Ouranopithecus, Paranthropus, Sivapithecus and Turkanapithecus) can be observed within a single extant hominoid subspecies, although generally with low probabilities. A resampling study is employed as a means for gauging the effect that this intrataxonomic variation may have on the consistency with which discrete orbital shape character states can be delimited given the small sample sizes available for most Miocene catarrhine taxa preserving this feature (i.e., n=1). For each type of morphometric variable, 100 cluster (UPGMA) analyses of pairwise ATDs are performed in which a single individual is randomly selected from each hominoid genus and analyzed alongside known extinct taxa; consensus trees are computed in order to obtain the frequencies with which different shape clusters appeared in each of the three analyses. The two major clusters appearing most frequently in all three consensus trees are found in only 57% (centroid variables), 49% (height-width variables), and 36% (EF variables) of these trees. If ranges of variation within represented extinct taxa could also be estimated, these frequencies would certainly be far lower. Hominoids clearly exhibit considerable intrageneric, intraspecific, and even intrasubspecific variation in orbit shape, and substantial morphometric overlap exists between taxa; consequently, discrete character states delimiting these patterns of continuous variation are likely to be highly unreliable in phylogenetic analyses of living and extinct species, particularly as the number of terminal taxa increases. Morphological phylogenetic studies of extant catarrhines that assess the effect of different methods (e.g., use of objective a priori weighting or frequency coding of variable characters, inclusion vs. exclusion of variable characters, use of specific vs. supraspecific terminal taxa) on phylogenetic accuracy may help to improve the techniques that systematists employ to make phylogenetic inferences about extinct taxa.     

Recent developments in the analysis of comparative data

Comparative methods can be used to test ideas about adaptation by identifying cases of either parallel or convergent evolutionary change across taxa. Phylogenetic relationships must be known or inferred if comparative methods are to separate the cross-taxonomic covariation among traits associated with evolutionary change from that attributable to common ancestry. Only the former can be used to test ideas linking convergent or parallel evolutionary change to some aspect of the environment. The comparative methods that are currently available differ in how they manage the effects brought about by phylogenetic relationships. One method is applicable only to discrete data, and uses cladistic techniques to identify evolutionary events that depart from phylogenetic trends. Techniques for continuous variables attempt to control for phylogenetic effects in a variety of ways. One method examines the taxonomic distribution of variance to identify the taxa within which character variation is small. The method assumes that taxa with small amounts of variation are those in which little evolutionary change has occurred, and thus variation is unlikely to be independent of ancestral trends. Analyses are then concentrated among taxa that show more variation, on the assumption that greater evolutionary change in the character has taken place. Several methods estimate directly the extent to which ancestry can predict the observed variation of a character, and subtract the ancestral effect to reveal variation of phylogeny. Yet another can remove phylogenetic effects if the true phylogeny is known. One class of comparative methods controls for phylogenetic effects by searching for comparative trends within rather than across taxa. With current knowledge of phylogenies, there is a trade-off in the choice of a comparative method: those that control phylogenetic effects with greater certainty are either less applicable to real data, or they make restrictive or untestable assumptions. Those that rely on statistical patterns to infer phylogenetic effects may not control phylogeny as efficiently but are more readily applied to existing data sets.     

Evaluating the efficacy of continuous quantitative characters for reconstructing the phylogeny of a morphologically homogeneous spider taxon (Araneae, Mygalomorphae, Antrodiaetidae, Antrodiaetus)

The use of continuous quantitative characters for phylogenetic analyses has long been contentious in the systematics literature. Recent studies argue for and against their use, but there have been relatively few attempts to evaluate whether these characters provide an accurate estimate of phylogeny, despite the fact that a number of methods have been developed to analyze these types of data for phylogenetic inference. A tree topology will be produced for a given methodology and set of characters, but little can be concluded with regards to the accuracy of phylogenetic signal without an independent evaluation of those characters. We assess the performance of continuous quantitative characters for the mygalomorph spider genus Antrodiaetus, a group that is morphologically homogeneous and one for which few discrete (morphological) characters have been observed. Phylogenetic signal contained in continuous quantitative characters is compared to an independently derived phylogeny inferred on the basis of multiple nuclear and mitochondrial gene loci. Tree topology randomizations, regression techniques, and topological tests all demonstrate that continuous quantitative characters in Antrodiaetus conflict with the phylogenetic signal contained in the gene trees. Our results show that the use of continuous quantitative characters for phylogenetic reconstruction may be inappropriate for reconstructing Antrodiaetus phylogeny and indicate that due caution should be exercised before employing this character type in the absence of other independently derived sources of characters.     

First cladistic analysis of the trilobite family Olenidae from the Furongian and Ordovician

The Olenidae stands out for its abundance and biostratigraphical importance, especially in the Lower Palaeozoic rocks of northwestern Argentina. Their phylogenetic relationships have been traditionally determined stratigraphically and by direct morphological comparison. This study reports the first formal phylogenetic analysis of olenids. Eighty‐six characters (24 quantitative and 62 qualitative) were coded for 65 taxa (58 olenids). Quantitative characters were treated both as discrete and as continuous variables. To explore the best way of character coding for this group, continuous characters were coded as: median, log‐median, normalized and rescaled. Maximum parsimony and implied weighting were used as optimality criteria. A phylogenetic hypothesis more consistent with traditional taxonomy was reconstructed with both quantitative and qualitative partitions. All the trees obtained with quantitative characters coded as continuous and rescaled are better resolved, and those topologies were more similar among them. This treatment also reflects more effectively the behaviour of the original variables. Olenidae is not a monophyletic clade: Andrarina costata and Aphelaspis australis are included within the ingroup, as sister clade of Olenus gibbosus. Also, the results suggest that members of the Hypermecaspidinae constitute a new family within the Order Olenida. The traditional taxonomic scheme at subfamily level is partially supported. Triarthrinae and ‘pelturinds’ are recovered as monophyletic clades, but Oleninae is polyphyletic. This study proves, through a formal cladistic analysis, that characters disregarded by traditional taxonomy can be uncovered. Finally, this is the first step towards achieving a classification of the Olenidae taking into account the evolutionary process involved in its diversification history.     

Character analysis in morphological phylogenetics: problems and solutions

Many aspects of morphological phylogenetics are controversial in the theoretical systematics literature and yet are often poorly explained and justified in empirical studies. In this paper, I argue that most morphological characters describe variation that is fundamentally quantitative, regardless of whether they are coded qualitatively or quantitatively by systematists. Given this view, three fundamental problems in morphological character analysis (definition, delimitation, and ordering of character states) may have a common solution: coding morphological characters as continuous quantitative traits. A new parsimony method (step-matrix gap-weighting, a modification of Thiele's approach) is proposed that allows quantitative traits to be analyzed as continuous variables. The problem of scaling or weighting quantitative characters relative to qualitative characters (and to each other) is reviewed, and three possible solutions are described. The new coding method is applied to data from hoplocercid lizards, and the results show the sensitivity of phylogenetic conclusions to different scaling methods. Although some authors reject the use of continuous, overlapping, quantitative characters in phylogenetic analysis, quantitative data from hoplocercid lizards that are coded using the new approach contain significant phylogenetic structure and exhibit levels of homoplasy similar to those seen in data that are coded qualitatively.     

Morphological disparity in theropod jaws: comparing discrete characters and geometric morphometrics

Disparity, the diversity of form and function of organisms, can be assessed from cladistic or phenetic characters, and from discrete characters or continuous characters such as landmarks, outlines, or ratios. But do these different methods of assessing disparity provide comparable results? Here we provide evidence that all metrics correlate significantly with each other and capture similar patterns of morphological variation. We compare three methods of capturing morphological disparity (discrete characters, geometric morphometric outlines and geometric morphometric landmarks) in coelurosaurian dinosaurs. We standardize our study by focusing all our metrics on the mandible, so avoiding the risk of confounding disparity methods with anatomical coverage of the taxa. The correlation is strongest between the two geometric morphometric methods, and weaker between the morphometric methods and the discrete characters. By using phylogenetic simulations of discrete character and geometric morphometric data sets, we show that the strength of these correlations is significantly greater than expected from the evolution of random data under Brownian motion. All disparity metrics confirm that Maniraptoriformes had the highest disparity of all coelurosaurians, and omnivores and herbivores had higher disparity than carnivores.     

Morphometric analysis of Alaskan members of the genus Potentilla sect. Niveae (Rosaceae)

A morphometric study of Potentilla nivea, P unijlora, and P hookeriana, as well as the close relative of the latter, P furcata, has been carried out, and the quantitative data subjected to Canonical Discriminant Analysis. The four taxa belong to the arctic-alpine section Niveae of Potentilla, and material for the analysis was collected in Alaska, U. S. A. The a priori defined groups are based on petiole hair type, the qualitative, and only, character traditionally used to distinguish taxa within Potentilla sect. Niveae. The hair types recognized previously by taxonomists have been vaguely defined, and the intraspecific variation of other morphological characters has never been discussed. Ordination by canonical discriminant analysis was performed to characterize mean differences among species, to obtain insight into group differences, and to estimate character weights from correlations between canonical variates and original variables. The four taxa differ significantly in the canonical analysis of six quantitative characters. Leaflet length, incision depth (length of leaflet teeth), and ovule number are shown to be the most important discriminators. A key to the four taxa, taking into account the intra- vesus interspecific variation, as well as character weights, is provided.     

Generalized frequency coding: a method of preparing polymorphic multistate characters for phylogenetic analysis

A new method of coding polymorphic multiistate characters for phylogenetic analysis is presented. By dividing such characters into subcharacters, their frequency distributions can be represented with discrete states. Differential weighting is used to counter the effect of representing one character with multiple characters. The new method, generalized frequency coding (GFC), is potentially superior to previously used methods in that it incorporates more information and is applicable to both qualitative and quantitative characters. When applied to a previously published data set that includes both types of polymorphic multistate characters, the method performed well, as assessed with g1 and nonparametric bootstrap statistics and giving results congruent with those of other studies. The data set was also used to compare GFC with both gap-weighting and Manhattan distance step matrix coding. On these grounds and for philosophical reasons, we consider GFC to be a better estimator of phylogeny.     

Signal, noise, and reliability in molecular phylogenetic analyses.

DNA sequences and other molecular data compared among organisms may contain phylogenetic signal, or they may be randomized with respect to phylogenetic history. Some method is needed to distinguish phylogenetic signal from random noise to avoid analysis of data that have been randomized with respect to the historical relationships of the taxa being compared. We analyzed 8,000 random data matrices consisting of 10-500 binary or four-state characters and 5-25 taxa to study several options for detecting signal in systematic data bases. Analysis of random data often yields a single most-parsimonious tree, especially if the number of characters examined is large and the number of taxa examined is small (both often true in molecular studies). The most-parsimonious tree inferred from random data may also be considerably shorter than the second-best alternative. The distribution of tree lengths of all tree topologies (or a random sample thereof) provides a sensitive measure of phylogenetic signal: data matrices with phylogenetic signal produce tree-length distributions that are strongly skewed to the left, whereas those composed of random noise are closer to symmetrical. In simulations of phylogeny with varying rates of mutation (up to levels that produce random variation among taxa), the skewness of tree-length distributions is closely related to the success of parsimony in finding the true phylogeny. Tables of critical values of a skewness test statistic, g1, are provided for binary and four-state characters for 10-500 characters and 5-25 taxa. These tables can be used in a rapid and efficient test for significant structure in data matrices for phylogenetic analysis.     

The Logical Basis for the use of Continuous Characters in Phylogenetic Systematics

It has been argued that continuous characteristics should be excluded from cladistic analysis for two reasons: because the data are considered inappropriate; and because the methods for the conversion of these data into codes are considered arbitrary. Metric data, however, fulfill the sole criterion for inclusion in phylogenetic analysis, the presence of homologous character states, and thus cannot be excluded as a class of data. The second line of reasoning, that coding methods are arbitrary, applies to gap and segment coding, but quantitative data can be coded in a nonarbitrary manner by means of tests of statistical significance. These procedures, which are both objective and repeatable, determine the probability that two taxa possess an homologous character state; that is, if they have inherited a particular central tendency and distribution of individual variates unchanged from a common ancestor. Thus, the application of statistical tests to quantitative data empirically detects the presence of evolu tionary change, the raw material of phylogenetic reconstruction.     

Principal component analysis as an alternative treatment for morphometric characters: phylogeny of caseids as a case study

In a recent study, the phylogeny of Caseidae (a herbivorous family of Palaeozoic synapsids belonging to the paraphyletic grade known as pelycosaurs) was analysed with a dataset employing more than three hundred continuous morphological characters in an effort to follow the principles of total evidence. Continuous characters are a source of great debate, with disagreements surrounding their suitability for and treatment in phylogenetic analysis. A number of shortcomings were identified in the handling of continuous characters in this study of caseids, including the use of gap weighting to discretize the characters and potential issues with redundancy and character non‐independence. Therefore, an alternative treatment for these characters is suggested here. First, rather than using gap weighting, the continuous characters were analysed in the program TNT, in which the raw values can be treated as continuous rather than discrete. Second, prior to the phylogenetic analysis, the continuous characters were subjected to a log‐ratio principal component analysis, and then the principal components were included in the character matrix rather than the raw ratios. Analysing the original data in TNT produced little difference in the results, but using the principal components as continuous characters resulted in alternative positions for Caseopsis agilis, Ennatosaurus tecton and Caseoides sanangeloensis. The differences are judged to be due to the reduced redundancy of the characters, the smaller number of principal components not overwhelming the discrete characters and the use of a scaling method which allows principal components with a higher variance to have a greater influence on the analysis. The positions of highly fragmentary fossils depended heavily on the method used to treat the missing characters in the principal component analysis, and so the method proposed here is not recommended for analysing very incomplete taxa.     

Quantitative morphology and species delimitation under the general lineage concept: Optimization for Hedera (Araliaceae)

? Premise of the study: The use of continuous morphological characters in taxonomy is traditionally contingent on the existence of discrete diagnostic characters. When plant species are the result of recent divergence and gene flow and/or hybridization occur, the use of continuous morphological characters may help in species identification and delimitation. Between nine and 15 species have been recognized in the last treatments of Hedera. The recent divergence of the species and the involvement of allopolyploidization as the main force in this process may have greatly impeded the establishment of clear limits and contributed to multiple taxonomic proposals. ? Methods: A multivariate statistical decision-making procedure was applied to 56 quantitative morphological characters and 602 specimens to identify and delimit Hedera species under the general lineage concept. Species' exclusive genetic ancestry was evaluated with the genealogical sorting index from the Bayesian inference trees of 30 Hedera ITS sequences. ? Key results: The decision-making procedure allowed recognizing 12 species and two groups (stellate and scale-like trichome groups) in Hedera and provided statistical support for making decisions about long-standing taxonomic controversies. Common ancestry was detected for the populations of three species even in the absence of the species monophyly. ? Conclusions: Quantitative variation supports discrete variation and provides statistical support for the taxa recognized in some recent proposals of Hedera. The need of explicit analysis of quantitative data are claimed to reduce taxonomic subjectivity and ease decision-making when qualitative data fail.     

Measuring the phylogenetic randomness of biological data sets

Two qualitative taxonomic characters are potentially compatible if the states of each can be ordered into a character state tree in such a way that the two resulting character state trees are compatible. The number of potentially compatible pairs (NPCP) of qualitative characters from a data set may be considered to be a measure of its phylogenetic randomness. The value of NPCP depends on the number of evolutionary units (EUs), the number of characters, the number of states in the characters, the distributions of EUs among these states, and the amount and distribution of missing information and so does not directly indicate degree of phylogenetic randomness. Thus, for an observed data set, we used Monte Carlo methods to estimate the probability that a data set chosen equiprobably from among those identical (with respect to all the other above determining features) to the observed data set would have as high (or low) an NPCP as the observed data set. This probability, the realized significance of the observed NPCP, is attractive as an indication of phylogenetic randomness because it does not require the assumptions made by other such methods: No character state trees are assumed and consequently, only potential compatibility can be determined; no particular method of phylogenetic estimation is assumed; and no phylogenetic trees are constructed. We determined the values and significances of NPCP for analyses of 57 data sets taken from 53 published sources. All data sets from 37 of those sources exhibited realized significances of < 0.01, indicating high levels of phylogenetic nonrandomness. From each of the remaining 16 sources, at least one data set was more phylogenetically random. Inclusion of outgroups changed significance in some cases, but not always in the same direction. Data sets with significantly low NPCP may be consistent with an ancient hybrid origin (or other ancient polyphyletic gene exchange, crossing over, viral transfer, etc.) of the study group.     

Problems with the use of cladistic analysis in palaeoanthropology

Cladistic analysis is a popular method for reconstructing evolutionary relationships on the human lineage. However, it has limitations and hidden assumptions that are often not considered by palaeoanthropologists. Some researchers who are opposed to its use regard cladistics as the preferred method for taxonomic «splitters» and claim it has lead to a revitalisation of typology. Typology remains a part of human evolutionary studies, regardless of the acceptance or use of cladistics. The assumption/preference for «splitting» over «lumping» in cladistics (alpha) taxonomy and the general failure to evaluate (post-hoc) such taxonomies have served to reinforce this assertion.

Researchers have also adopted a number of practices that are logically untenable or introduce considerable error. The evolutionary trend of human encephalisation, apparently isometric with body size, and concurrent reduction in the gut and masticatory apparatus, suggests continuous cladistic characters are biased by problems of body size.

The method suffers a logical weakness, or circularity, leading to bias when characters with multiple states are used. Coding of such characters can only be done using prior criteria, and this is usually done using an existing phylogenetic scheme. Another problem with coding character states is the handling of variation within species. While this form of variation is usually ignored by palaeoanthropologists, when characters are recognised as varying, their treatment as a separate state adds considerable error to cladograms.

The genetic proximity of humans, chimpanzees and gorillas has important implications for cladistic analyses. It is argued that chimpanzees and gorillas should be treated as ingroup taxa and an alternative outgroup such as orangutans should be used, or an (hypothetical) ancestral body plan developed. Making chimpanzees and gorillas ingroup taxa would considerably enhance the biological utility of anthropological cladograms.

All published human cladograms fail to meet standard quality criteria indicating that none of them may be considered reliable. The continuing uncertainty over the number and composition of fossil human species is the largest single source of error for cladistics and human phylogenetic reconstruction.