Evidence for speciational change in the evolution of ratites (Aves: Palaeognathae)

To perform a comparative analysis of character associations framed in a phylogenetic context (e.g. independent contrasts), a model of character evolution must be assumed. According to phyletic gradualism, morphological change accumulates gradually over time within lineages, and speciation events do not have a major role. Under speciational models, morphological change is assumed to occur during or just after cladogenesis in both daughter species, and the resulting morphologies do not change over long periods of time (stasis), until the next cladogenetic event. A novel method is presented for comparing these models of character evolution that uses permutational multiple phylogenetic regressions. The addition of divergence times to well-corroborated phylogenetic trees and the utilization of the method developed in this paper allows the estimation of relative frequency of gradual change and speciational change from living organisms. This method is applied to a dataset from ratites with the conclusion that, for a range of morphological features, change tends to have been speciational rather than gradual.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 99–106.     

TESTING FOR UNEQUAL AMOUNTS OF EVOLUTION IN A CONTINUOUS CHARACTER ON DIFFERENT BRANCHES OF A PHYLOGENETIC TREE USING LINEAR AND SQUARED-CHANGE PARSIMONY: AN EXAMPLE USING LESSER ANTILLEAN ANOLIS LIZARDS

Although a large body of work investigating tests of correlated evolution of two continuous characters exists, hypotheses such as character displacement are really tests of whether substantial evolutionary change has occurred on a particular branch or branches of the phylogenetic tree. In this study, we present a methodology for testing such a hypothesis using ancestral character state reconstruction and simulation. Furthermore, we suggest how to investigate the robustness of the hypothesis test by varying the reconstruction methods or simulation parameters. As a case study, we tested a hypothesis of character displacement in body size of Caribbean Anolis lizards. We compared squared-change, weighted squared-change, and linear parsimony reconstruction methods, gradual Brownian motion and speciational models of evolution, and several resolution methods for linear parsimony. We used ancestor reconstruction methods to infer the amount of body size evolution, and tested whether evolutionary change in body size was greater on branches of the phylogenetic tree in which a transition from occupying a single-species island to a two-species island occurred. Simulations were used to generate null distributions of reconstructed body size change. The hypothesis of character displacement was tested using Wilcoxon Rank-Sums. When tested against simulated null distributions, all of the reconstruction methods resulted in more significant P-values than when standard statistical tables were used. These results confirm that P-values for tests using ancestor reconstruction methods should be assessed via simulation rather than from standard statistical tables. Linear parsimony can produce an infinite number of most parsimonious reconstructions in continuous characters. We present an example of assessing the robustness of our statistical test by exploring the sample space of possible resolutions. We compare ACCTRAN and DELTRAN resolutions of ambiguous character reconstructions in linear parsimony to the most and least conservative resolutions for our particular hypothesis.     

Speciational evolution of coloration in the genus Carduelis

Sexual selection has been hypothesized to promote speciation, but evidence relating sexual selection to differences in speciation rates among taxa is equivocal. We note that evolutionary changes in ornaments are the link connecting sexual selection to speciation, and that ornament evolution is influenced by many factors so that its relationship with the strength of sexual selection may not be linear. We test if the evolution of ornamental coloration in Carduelis finches is related with speciation and if more ornamented lineages speciate more. We found that coloration evolves with a speciational pattern, but we found no evidence that the evolutionary changes associated with speciation are predominantly gains in ornamentation. The speciational pattern was found for both carotenoid- and melanin-based coloration, suggesting that traits putatively under stronger sexual selection by female choice (carotenoid coloration) are not the sole ones facilitating reproductive isolation. We conclude that in the genus Carduelis the evolutionary lability of ornaments influences speciation more than the strength of sexual selection, and we suggest that ornament lability should be considered as a possible causal factor in studies comparing cladogenesis among taxa.     

Comparative methods for examining adaptation depend on evolutionary models

Comparisons among taxa provide a powerful means for helping to understand why primate species differ from each other in morphology, behaviour and life history. Comparative tests can also mislead when not applied correctly, and correct application means taking into account the phylogenetic relationships among the species being compared. Adaptation is defined as a comparative concept. The reasons for phenotypic similarity among closely related taxa are summarized. Different models of evolutionary change dictate different methods for reconstructing ancestral character states and for performing comparative analyses on categorical and continuously varying character. All comparative methods rely either implicitly of explicitly on some model of how evolution proceeds. The choice of a particular method of analysis is, therefore, an implicit choice of a model of evolution.     

Mapping uncertainty and phylogenetic uncertainty in ancestral character state reconstruction: an example in the moss genus Brachytheciastrum

The evolution of species traits along a phylogeny can be examined through an increasing number of possible, but not necessarily complementary, approaches. In this paper, we assess whether deriving ancestral states of discrete morphological characters from a model whose parameters are (i) optimized by ML on a most likely tree; (II) optimized by ML onto each of a Bayesian sample of trees; and (III) sampled by a MCMC visiting the space of a Bayesian sample of trees affects the reconstruction of ancestral states in the moss genus Brachytheciastrum. In the first two methods, the choice of a single- or two-rate model and of a genetic distance (wherein branch lengths are used to determine the probabilities of change) or speciational (wherein changes are only driven by speciation events) model based upon a likelihood-ratio test strongly depended on the sampled trees. Despite these differences in model selection, reconstructions of ancestral character states were strongly correlated to each others across nodes, often at r > 0.9, for all the characters. The Bayesian approach of ancestral character state reconstruction offers, however, a series of advantages over the single-tree approach or the ML model optimization on a Bayesian sample of trees because it does not involve restricting model parameters prior to reconstructing ancestral states, but rather allows a range of model parameters and ancestral character states to be sampled according to their posterior probabilities. From the distribution of the latter, conclusions on trait evolution can be made in a more satisfactorily way than when a substantial part of the uncertainty of the results is obscured by the focus on a single set of model parameters and associated ancestral states. The reconstructions of ancestral character states in Brachytheciastrum reveal rampant parallel morphological evolution. Most species previously described based on phenetic grounds are thus resolved of polyphyletic origin. Species polyphylly has been increasingly reported among mosses, raising severe reservations regarding current species definition.     

A likelihood method for detecting trait-dependent shifts in the rate of molecular evolution

Rate heterogeneity within groups of organisms is known to exist even when closely related taxa are examined. A wide variety of phylogenetic and dating methods have been developed that aim either to test for the existence of rate variation or to correct for its bias. However, none of the existing methods track the evolution of features that account for observed rate heterogeneity. Here, we present a likelihood model that assumes that rate variation is caused, in part, by species' intrinsic characteristics, such as a particular life-history trait, morphological feature, or habitat association. The model combines models of sequence and character state evolution such that rates of sequence change depend on the character state of a lineage at each point in time. We test, using simulations, the power and accuracy of the model to determine whether rates of molecular evolution depend on a particular character state and demonstrate its utility using an empirical example with halophilic and freshwater daphniids.     

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.     

Misinformative characters and phylogeny shape

The discrepancy between theoretical and observed distributions of tree shapes in recent surveys of phylogeny estimates has lead to investigations of possible biological and methodological causes. I investigated whether the phylogenetic quality of characters is related to the tree shape on which they evolve. Simulated evolution revealed shape-related tendencies for characters to indicate correct cladistic relationships; these differences were measured by examining the characters directly, without deriving any phylogeny estimates. Tree stemminess indices correlated strongly with character quality when characters evolved either speciationally or phyletically. Tree balance was a significant correlate of character quality under speciational evolution but not under phyletic evolution. These results help explain the findings of other simulation studies. With additional study of the behavior of evolving characters and their interaction with phylogenetic methods, we might be able to increase the accuracy of tree estimation and compensate for potential biases related to shape. These results give further reason for caution in trusting phylogeny estimates.     

Linking the investigations of character evolution and species diversification

Variation in diversification rates is often studied by investigating traits related to species' ecology and life history. Often, however, it is unknown whether these traits evolve gradually or in punctuated bursts during speciation. Using phylogenetic data and species' present-day trait information, we present a novel approach to assessing the mode of character change while accounting for trait-dependent speciation and extinction. Our model, "Binary-State Speciation and Extinction-node enhanced state shift" (BiSSE-ness), estimates both the rate of change occurring along lineages and the probability of change occurring during speciation, as well as independent speciation and extinction rates for each character state. Using simulations, we found that BiSSE-ness is able to distinguish along-lineage and speciational change and accurately estimate the parameters associated with character change and diversification rates. We applied BiSSE-ness to an empirical primate data set and found evidence for along-lineage changes in primate mating systems and social behaviors, whereas shifts in habitat were associated with speciation. In cases where trait changes may be linked to the speciation process itself (e.g., niche-related traits), BiSSE-ness provides a suitable framework with which to simultaneously address questions regarding species diversification and character change.     

The evolution of feather coloration and song in Old World orioles (genus Oriolus)

What is the tempo and mode of evolution – how fast and in what pattern do traits evolve – is a major question of evolutionary biology. Here we studied patterns of evolutionary change in visual and acoustic signals in Old World orioles. Since producing multiple signals may be costly, we also tested whether there was an evolutionary trade‐off between the elaboration of those two types of signals. We studied 30 Oriolus taxa using comparative methods and a recent molecular phylogeny. Morphology and plumage hue evolved comparatively slowly, whereas song evolved rapidly. Among individual feather patches, the evolutionary rate of color was slowest in primaries, which are critical for flapping flight, and fastest in patches exposed to observers (mantle and breast). Thus, primaries seem to be under functional constraint while the evolution of visually exposed patches is perhaps shaped by sexual selection. Song evolution was comparatively fast, but also attracted to a single optimum. This may be due to selection for signal efficacy, because all orioles inhabit similar forested habitats. Only color diversity was best fit by a speciational model: the biggest changes in coloration were concentrated at speciation events, thus perhaps linked to the evolution of species recognition. Our analysis did not reveal any evolutionary trade‐off between acoustic and visual signals, suggesting that the elaboration of visual and acoustic signals in the Old World orioles evolved independently. Our study shows that patterns of evolutionary change may be surprisingly complex even within a single clade of birds and thus further studies are needed to identify general patterns of signal macroevolution.     

Escaping from the Felsenstein Zone by Detecting Long Branches in Phylogenetic Data

Long branches in a true phylogeny tend to disrupt hierarchical character covariation (phylogenetic signal) in the distribution of traits among organisms. The distortion of hierarchical structure in character-state matrices can lead to errors in the estimation of phylogenetic relationships and inconsistency of methods of phylogenetic inference. Examination of trees distorted by long-branch attraction will not reveal the identities of problematic taxa, in part because the distortion can mask long branches by reducing inferred branch lengths and through errors in branching order. Here we present a simple method for the detection of taxa whose placement in evolutionary trees is made difficult by the effects of long-branch attraction. The method is an extension of a tree-independent conceptual framework of phylogenetic data exploration (RASA). Taxa that are likely to attract are revealed because long branches leave distinct footprints in the distribution of character states among taxa, and these traces can be directly observed in the error structure of the RASA regression. Problematic taxa are identified using a new diagnostic plot called the taxon variance plot, in which the apparent cladistic and phenetic variances contributed by individual taxa are compared. The procedure for identifying long edges employs algorithms solved in polynomial time and can be applied to morphological, molecular, and mixed characters. The efficacy of the method is demonstrated using simulated evolution and empirical evidence of long branches in a set of recently published sequences. We show that the accuracy of evolutionary trees can be improved by detecting and combating the potentially misleading influences of long-branch taxa.     

The phylogenetic interpretation of biological surveys

The ecological attributes of two species may be similar through convergent evolution or common ancestry. The extent of similarity by descent can be evaluated by comparing them with their most closely‐related outgroup in a given phylogeny. I describe a method of nested sister‐group analysis for estimating ecological similarity based on landscape features or on co‐distribution. The phylogeny is dissected into triplets, each comprising two sister taxa and their outgroup. For a triplet at any phylogenetic level, the similarity of sister groups with respect to some given character can be compared with their joint similarity to the outgroup to give a single test of similarity by descent. Each comparison is independent, and the full set of triplets provides a complete accounting of phylogenetic variation at all levels. This procedure was applied to 188 moderately abundant species of dicots in two independent surveys from adjoining districts of midland England, supplemented by physical surveys of landscape attributes obtained from digitized maps of the same districts. The co‐distribution of sister species was consistently more positive than the co‐distribution of random species pairs, demonstrating the existence of a phylogenetic signal at some level. When sister species are compared with their most closely‐related outgroup, however, neither landscape attributes nor co‐distribution showed any overall similarity arising from common ancestry, in the sense that ecological attributes are not generally conserved after lineage splitting. Instead, the distribution of similarity is strikingly similar to random data. The lack of ecological similarity between closely‐related groups was attributed to rapid character change at or shortly after the splitting of lineages, coupled with a lack of correlation between successive lineage splits.     

PHYLOGENIES AND THE ANALYSIS OF EVOLUTIONARY SEQUENCES,WITH EXAMPLES FROM SEED PLANTS

Studies of character evolution have frequently relied on ahistorical correlations rather than on phylogenies. However, correlations do not estimate the number of times that a trait evolved, and they are insensitive to the direction or the temporal sequence of character transformation. In contrast, cladograms can provide this information. A cladistic test of the hypothesis that the evolution of dioecy is favored in animal-dispersed plants indicates that dioecy may have originated somewhat more often in such lineages. Nevertheless, differences in rates of speciation or extinction must largely account for the observed species-level correlation between dispersal and breeding system. In considering the evolution of individual traits, cladograms help identify the context in which a feature evolved and specify which organisms should be compared in evaluating the causes of character change. Determining whether a feature and a performance advantage were strictly historically correlated or followed one another in sequence helps to distinguish whether the trait is an adaptation or an exaptation for the function. For example, cladograms of seed plants suggest that double fertilization arose incidentally prior to the origin of angiosperms and that the resulting product was later co-opted and elaborated as a nutritive tissue for the developing embryo. The order of character assembly in a lineage also bears on the evolution of functional and developmental interdependencies. In particular, it may be possible to trace the evolution of a character's “burden” from an initial period, during which change is more likely, through later stages, wherein successful modification is less likely owing to the evolution of dependent characters. The evolution of vessels and of floral phyllotaxis in angiosperms may exemplify this pattern. Recognition that the likelihood of character transformation may change during the evolution of a group warns against character weighting in phylogenetic analysis.     

A comparison of numerical and biosystematic studies in Haplopappus

Numerical phenetics, based on indiscriminate choice of characters and equal weighting, does not directly reflect cladistic or lineage relationships in some taxa ofHaplopappus. However, the degree to which the lineage and phenetic relationships diverge may be used as an assay of the amount of parallel evolution that has occurred. Several numerical taxonomic methods were employed. For each method a change in the number of characters from 31 to 29, by deletion of two karyotypic characters, yielded a significant change in the results. Uses of numerical techniques for the study of character dines and adaptive character complexes are discussed.     

PATTERNS OF VARIATION IN LEVELS OF HOMOPLASY

Patterns of variation in levels of homoplasy were explored through statistical analyses of standardized consistency indexes. Data were obtained from 60 recent cladistic analyses of a wide variety of organisms based on several different kinds of characters. Consistency index is highly correlated with the number of taxa included in an analysis, with homoplasy increasing as the number of taxa increases. This observation is compatible with a simple model of character evolution in which 1) the probability of character-state change increases with the total number of branches in a tree and 2) the number of possible states of a character is limited. Consistency index does not show a significant relationship to the number of characters utilized in an analysis or to the taxonomic rank of the terminal taxa. When the relationship between consistency index and number of taxa is taken into account, there is no significant difference between plant and animal data sets in the amount of homoplasy. Likewise, the level of homoplasy in morphological and molecular data sets does not appear to differ significantly, although there are still too few molecular studies to be confident of this result. Future comparisons of consistency indexes, including studies along the lines established here, must take into account the influence of the number of taxa on homoplasy.     

Inferring and testing hypotheses of cladistic character dependence by using character compatibility

The notion that two characters evolve independently is of interest for two reasons. First, theories of biological integration often predict that change in one character requires complementary change in another. Second, character independence is a basic assumption of most phylogenetic inference methods, and dependent characters might confound attempts at phylogenetic inference. Previously proposed tests of correlated character evolution require a model phylogeny and therefore assume that nonphylogenetic correlation has a negligible effect on initial tree construction. This paper develops "tree-free" methods for testing the independence of cladistic characters. These methods can test the character independence model as a hypothesis before phylogeny reconstruction, or can be used simply to test for correlated evolution. We first develop an approach for visualizing suites of correlated characters by using character compatibility. Two characters are compatible if they can be used to construct a tree without homoplasy. The approach is based on the examination of mutual compatibilities between characters. The number of times two characters i and j share compatibility with a third character is calculated, and a pairwise shared compatibility matrix is constructed. From this matrix, an association matrix analogous to a dissimilarity matrix is derived. Eigenvector analyses of this association matrix reveal suites of characters with similar compatibility patterns. A priori character subsets can be tested for significant correlation on these axes. Monte Carlo tests are performed to determine the expected distribution of mutual compatibilities, given various criteria from the original data set. These simulated distributions are then used to test whether the observed amounts of nonphylogenetic correlation in character suites can be attributed to chance alone. We have applied these methods to published morphological data for caecilian amphibians. The analyses corroborate instances of dependent evolution hypothesized by previous workers and also identify novel partitions. Phylogenetic analysis is performed after reducing correlated suites to single characters. The resulting cladogram has greater topological resolution and implies appreciably less change among the remaining characters than does a tree derived from the raw data matrix.     

Evolutionary Diversification of Continuous Traits: Phylogenetic Tests and Application to Seed Size in the California Flora

Evolutionary diversification of a phenotypic trait reflects the tempo and mode of trait evolution, as well as the phylogenetic topology and branch lengths. Comparisons of trait variance between sister groups provide a powerful approach to test for differences in rates of diversification, controlling for differences in clade age. We used simulation analyses under constant rate Brownian motion to develop phylogenetically based F-tests of the ratio of trait variances between sister groups. Random phylogenies were used for a generalized evolutionary null model, so that detailed internal phylogenies are not required, and both gradual and speciational models of evolution were considered. In general, phylogenetically structured tests were more conservative than corresponding parametric statistics (i.e., larger variance ratios are required to achieve significance). The only exception was for comparisons under a speciational evolutionary model when the group with higher variance has very low sample size (number of species). The methods were applied to a large data set on seed size for 1976 species of California flowering plants. Seven of 37 sister-group comparisons were significant for the phylogenetically structured tests (compared to 12 of 37 for the parametric F-test). Groups with higher diversification of seed size generally had a greater diversity of fruit types, life form, or life history as well. The F-test for trait variances provides a simple, phylogenetically structured approach to test for differences in rates of phenotypic diversification and could also provide a valuable tool in the study of adaptive radiations.     

Song and plumage evolution in the New World orioles (Icterus) show similar lability and convergence in patterns

Both song and color patterns in birds are thought to evolve rapidly and exhibit high levels of homoplasy, yet few previous studies have compared the evolution of these traits systematically using the same taxa. Here we reconstruct the evolution of song in the New World orioles (Icterus) and compare patterns of vocal evolution to previously reconstructed patterns of change in plumage evolution in this clade. Individual vocal characters exhibit high levels of homoplasy, reflected in a low overall consistency index (CI = 0.27) and retention index (RI = 0.35). Levels of lability in song are comparable to those found for oriole plumage patterns using the same taxa (CI = 0.31, RI = 0.63), but are strikingly dissimilar to the conservative patterns of change seen in the songs of oropendolas (Psarocolius, Ocyalus; CI = 0.82, RI = 0.87), a group closely related to the orioles. Oriole song is also similar to oriole plumage in exhibiting repeated convergence in overall patterns, with some distantly related taxa sounding remarkably similar. Thus, both song and plumage in orioles show repeated convergence in individual elements and in overall patterns across the clade, suggesting that both of these character classes are highly labile between taxa yet highly conserved within the genus. Our results provide new insights into the tempo and mode of evolution in sexually selected traits within and across clades.     

NULL MODELS FOR THE NUMBER OF EVOLUTIONARY STEPS IN A CHARACTER ON A PHYLOGENETIC TREE

Random trees and random characters can be used in null models for testing phylogenetic hypothesis. We consider three interpretations of random trees: first, that trees are selected from the set of all possible trees with equal probability; second, that trees are formed by random speciation or coalescence (equivalent); and third, that trees are formed by a series of random partitions of the taxa. We consider two interpretations of random characters: first, that the number of taxa with each state is held constant, but the states are randomly reshuffled among the taxa; and second, that the probability each taxon is assigned a particular state is constant from one taxon to the next. Under null models representing various combinations of randomizations of trees and characters, exact recursion equations are given to calculate the probability distribution of the number of character state changes required by a phylogenetic tree. Possible applications of these probability distributions are discussed. They can be used, for example, to test for a panmictic population structure within a species or to test phylogenetic inertia in a character's evolution. Whether and how a null model incorporates tree randomness makes little difference to the probability distribution in many but not all circumstances. The null model's sense of character randomness appears more critical. The difficult issue of choosing a null model is discussed.