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.     

Phenotypic plasticity: an evolving plant character

Phenotypic plasticity is an important mode of adaptation to temporal and spatial environmental variability, particularly in plants. Although data are available concerning interspecific differences in the sizes and shapes of characters, there is little information concerning differences between taxa for the plastic responses of those characters. We have measured: (1) the mean value of a character, (2) the amount of character plasticity, and (3) the pattern of phenotypic plasticity for species in five genera, and calculated the divergences among species for each of these three measures. We compared the divergences of these measures to address the question of whether there is a relationship between the evolution of the character means of species and the evolution of the plasticities of those characters. We found that the evolutionary divergence of character plasticities could be independent of the interspecific divergence of character means. There was, however, a tendency for the divergence of amounts and patterns of plasticity to be related.     

Chromosomal evolution in Rodentia

Rodentia is the most species-rich mammalian order and includes several important laboratory model species. The amount of new information on karyotypic and phylogenetic relations within and among rodent taxa is rapidly increasing, but a synthesis of these data is currently lacking. Here, we have integrated information drawn from conventional banding studies, recent comparative painting investigations and molecular phylogenetic reconstructions of different rodent taxa. This permitted a revision of several ancestral karyotypic reconstructions, and a more accurate depiction of rodent chromosomal evolution.     

ANCESTRAL CHARACTER ESTIMATION UNDER THE THRESHOLD MODEL FROM QUANTITATIVE GENETICS

Evolutionary biology is a study of life's history on Earth. In researching this history, biologists are often interested in attempting to reconstruct phenotypes for the long extinct ancestors of living species. Various methods have been developed to do this on a phylogeny from the data for extant taxa. In the present article, I introduce a new approach for ancestral character estimation for discretely valued traits. This approach is based on the threshold model from evolutionary quantitative genetics. Under the threshold model, the value exhibited by an individual or species for a discrete character is determined by an underlying, unobserved continuous trait called “liability.” In this new method for ancestral state reconstruction, I use Bayesian Markov chain Monte Carlo (MCMC) to sample the liabilities of ancestral and tip species, and the relative positions of two or more thresholds, from their joint posterior probability distribution. Using data simulated under the model, I find that the method has very good performance in ancestral character estimation. Use of the threshold model for ancestral state reconstruction relies on a priori specification of the order of the discrete character states along the liability axis. I test the use of a Bayesian MCMC information theoretic criterion based approach to choose among different hypothesized orderings for the discrete character. Finally, I apply the method to the evolution of feeding mode in centrarchid fishes.     

Evolutionary analysis identifies multiple genome expansions and contractions in Sepsidae (Diptera) and suggests targets for future genomic research

We here argue that data from comparative studies of genome size and karyotypes provide important information for planning comparative research on genome evolution. We document for 39 species of sepsids that there is a four‐fold difference in genome size (151–618 Mbp). Mapping genome sizes onto a phylogenetic hypothesis identifies that this range is the result of five genome expansions and four genome contractions that we here define as changes in genome size of more than 50 Mbp. We then generate karyotype data for 10 species and find no changes in chromosome number. The study reveals that the “Oriental” clade of sepsids is a promising system for studying genome evolution because it has experienced three genome expansion events. These events can be compared with an expansion in the “Neotropical” clade in order to reveal the mechanisms that underlie genome expansion in Sepsidae. A review of the literature on genome sizes and karyotypes reveals that they have been poorly documented in Metazoa. This means that researchers interested in the evolution of genome expansions and contractions are currently not being able to identify appropriate target taxa for genome sequencing. We thus argue for more comparative research on genome sizes and karyotypes and point out that historically species were chosen for genome sequencing for reasons not related to genome evolution (e.g. small genome size, model species status, phylogenetic position, interesting phenotypes). We believe that it is now time to use a more genome‐centric selection criterion, where species for whole genome sequencing are selected based on their importance for understanding genome evolution.     

Avian louse phylogeny (Phthiraptera: Ischnocera): a cladistic study based on morphology

The louse suborder Ischnocera (Phthiraptera) contains 3060 currently described species from over 150 genera. These lice are permanent obligatory ectoparasites of a diverse selection of birds and mammals with a worldwide distribution. Historically, they have played a major role in the development of our ideas on coevolution, and species hosted by mammals have been used extensively as model organisms for the study of cospeciation. In contrast, avian taxa comprising 90% of ischnoceran species have been neglected due to a lack of data on their wider systematics. A comparative study based on the adult and nymphal instar morphology of avian lice yielded 138 characters from 56 species (51 genera), all of which are illustrated or discussed here for the first time. A further five outgroup taxa were examined from the mammalian ischnoceran family Trichodectidae. Phylogenetic analyses of these data produced three most parsimonious cladograms, the strict consensus of which is highly resolved and broadly consistent with previous classifications. Morphological character variation is extensive, and nymphal character traits are useful in identifying instances of convergent evolution in adult morphology. The role of ontogeny in the development of the major character complexes of the head and abdomen is discussed, and its implications for further work on the phylogeny of avian Ischnocera is considered. Comparison with host taxonomy reveals a series of complex host-parasite associations that do not support a hypothesis of strict one to one cospeciation. However, extrapolation of these associations is compromised by the low sample size. The role of niche specialization to explain the presence of multiple unrelated lineages on the same host taxon is considered.     

Comparative analyses for adaptive radiations

Biologists generally agree that most morphological variation between closely related species is adaptive. The most common method of comparative analysis to test for co-evolved character variation is based on a Brownian-motion model of character evolution. If we are to test for the evolution of character-covariation, and we believe that characters have evolved adaptively to fill niches during an adaptive radiation, then it is appropriate to employ appropriate models for character evolution. We show here that under several models of adaptive character evolution and coevolution during an adaptive radiation, which result in closely related species being more similar to each other than to more distantly related species, cross-species analyses are statistically more appropriate than contrast analyses. If the evolution of some traits fits the Brownian-motion model, while others evolve to fill niches during an adaptive radiation, it might be necessary to identify the number of relevant niche dimensions and the modes of character evolution before deciding on appropriate statistical procedures. Alternatively, maximum-likelihood procedures might be used to determine appropriate transformations of phylogenetic branch lengths that accord with particular models of character evolution.     

MIPoD: a hypothesis-testing framework for microevolutionary inference from patterns of divergence

Despite the many triumphs of comparative biology during the past few decades, the field has remained strangely divorced from evolutionary genetics. In particular, comparative methods have failed to incorporate multivariate process models of microevolution that include genetic constraint in the form of the G matrix. Here we explore the insights that might be gained by such an analysis. A neutral model of evolution by genetic drift that depends on effective population size and the G matrix predicts a probability distribution for divergence of population trait means on a phylogeny. Use of a maximum likelihood (ML) framework then allows us to compare independent direct estimates of G with the ML estimates based on the observed pattern of trait divergence among taxa. We assess the departure from neutrality, and thus the role of different types of selection and other forces, in a stepwise hypothesis-testing procedure based on parameters for the size, shape, and orientation of G. We illustrate our approach with a test case of data on vertebral number evolution in garter snakes.     

THE QUANTITATIVE ASSESSMENT OF PHYLOGENETIC CONSTRAINTS IN COMPARATIVE ANALYSES: SEXUAL DIMORPHISM IN BODY WEIGHT AMONG PRIMATES

We have presented a formal model for the quantitative analysis of phylogenetic and specific effects on the distribution of trait values among species. Total trait values are divided into phylogenetic values, inherited from an ancestral species, and specific values, the result of independent evolution. This allows a quantitative assessment of the strength of the phylogenetic inertia, or burden, displayed by a character in a lineage, so that questions concerning the relative importance of phylogenetic constraints in evolution can be answered. The separation of phylogenetic from specific effects proposed here also allows phylogenetic factors to be explicitly included in cross-species comparative analyses of adaptation. This solves a long-standing problem in evolutionary comparative studies. Only species' specific values can provide information concerning the independent evolution of characters in a set of related species. Therefore, only correlations among specific values for traits may be used as evidence for adaptation in cross-species comparative analyses. The phylogenetic autocorrelation model was applied to a comparative analysis of the determinants of sexual dimorphism in weight among 44 primate species. In addition to sexual dimorphism in weight, mating system, habitat, diet, and size (weight itself) were included in the analysis. All of the traits, except diet, were substantially influenced by phylogenetic inertia. The comparative analysis of the determinants of sexual dimorphism in weight indicates that 50% of the variation among primate species is due to phylogeny. Size, or scaling, could account for a total of 36% of the variance, making it almost as important as phylogeny in determining the level of dimorphism displayed by a species. Habitat, mating system, and diet follow, accounting for minor amounts of variation. Thus, in attempting to explain why a particular modern primate species is very dimorphic compared to other primates, we would say first because its ancestor was more dimorphic than average, second because it is a relatively large species, and third because it is terrestrial, polygynous, and folivorous.     

Identifying species of moths (Lepidoptera) from Baihua Mountain,Beijing, China,using DNA barcodes

DNA barcoding has become a promising means for the identification of organisms of all life‐history stages. Currently, distance‐based and tree‐based methods are most widely used to define species boundaries and uncover cryptic species. However, there is no universal threshold of genetic distance values that can be used to distinguish taxonomic groups. Alternatively, DNA barcoding can deploy a “character‐based” method, whereby species are identified through the discrete nucleotide substitutions. Our research focuses on the delimitation of moth species using DNA‐barcoding methods. We analyzed 393 Lepidopteran specimens belonging to 80 morphologically recognized species with a standard cytochrome c oxidase subunit I (COI) sequencing approach, and deployed tree‐based, distance‐based, and diagnostic character‐based methods to identify the taxa. The tree‐based method divided the 393 specimens into 79 taxa (species), and the distance‐based method divided them into 84 taxa (species). Although the diagnostic character‐based method found only 39 so‐identifiable species in the 80 species, with a reduction in sample size the accuracy rate substantially improved. For example, in the Arctiidae subset, all 12 species had diagnostics characteristics. Compared with traditional morphological method, molecular taxonomy performed well. All three methods enable the rapid delimitation of species, although they have different characteristics and different strengths. The tree‐based and distance‐based methods can be used for accurate species identification and biodiversity studies in large data sets, while the character‐based method performs well in small data sets and can also be used as the foundation of species‐specific biochips.     

The accuracy of methods for coding and sampling higher-level taxa for phylogenetic analysis: a simulation study

Many phylogenetic analyses, particularly morphological studies, use higher taxa (e.g., genera, families) rather than species as terminal taxa. This general approach requires dealing with interspecific variation among the species that make up the higher taxon. In this paper, I review different parsimony methods for coding and sampling higher taxa and compare their relative accuracies using computer simulations. Despite their widespread use, methods that involve coding higher taxa as terminals perform poorly in simulations, relative to splitting up the higher taxa and using species as terminals. Among the methods that use higher taxa as terminals, coding a taxon based on the most common condition among the included species (majority or modal coding) is generally more accurate than other coding methods, such as coding taxa as missing or polymorphic. The success of the majority method, and results of further simulations, suggest that in many cases "common equals primitive" within variable taxa, at least for low and intermediate rates of character change. The fixed-only method (excluding variable characters) performs very poorly, a result that is indirectly supported by analyses of published data for squamate reptiles. Sampling only a single species per higher taxon also yields low accuracy under many conditions. Along with recent studies of intraspecific polymorphism, the results of this study show the general importance of (1) including characters despite variation within taxa and (2) using methods that incorporate detailed information on the distribution of states within variable taxa.     

Life history evolution and comparative developmental biology of echinoderms

Evolutionary biologists studying life history variation have used echinoderms in experimental, laboratory, and field studies of life history evolution. This focus on echinoderms grew originally from the tradition of comparative embryology, in which echinoderms were central. The tools for obtaining and manipulating echinoderm gametes and larvae were taken directly from comparative embryological research. In addition, the comparative embryologists employed a diverse array of echinoderms, not a few model species, and this diversity has led to a broad understanding of the development, function, and evolution of echinoderm larvae. As a result, this branch of life history evolution has deep roots in comparative developmental biology of echinoderms. Here two main aspects of this relationship are reviewed. The first is a broad range of studies of fertilization biology, dispersal, population genetics, functional morphology, and asexual reproduction in which developmental biologists might take a keen interest because of the historical origins of this research in echinoderm comparative embryology. The second is a similarly broad variety of topics in life history research in which evolutionary biologists require techniques or data from developmental biology in order to make progress on understanding patterns of life history variation among echinoderm species and higher taxa. Both sets of topics provide opportunities for interaction and collaboration.     

How phylogeny and foraging ecology drive the level of chemosensory exploration in lizards and snakes

The chemical senses are crucial for squamates (lizards and snakes). The extent to which squamates utilize their chemosensory system, however, varies greatly among taxa and species’ foraging strategies, and played an influential role in squamate evolution. In lizards, ‘Scleroglossa’ evolved a state where species use chemical cues to search for food (active foragers), whereas ‘Iguania’ retained the use of vision to hunt prey (ambush foragers). However, such strict dichotomy is flawed as shifts in foraging modes have occurred in all clades. Here, we attempted to disentangle effects of foraging ecology from phylogenetic trait conservatism as leading cause of the disparity in chemosensory investment among squamates. To do so, we used species’ tongue‐flick rate (TFR) in the absence of ecological relevant chemical stimuli as a proxy for its fundamental level of chemosensory investigation, that is baseline TFR. Based on literature data of nearly 100 species and using phylogenetic comparative methods, we tested whether and how foraging mode and diet affect baseline TFR. Our results show that baseline TFR is higher in active than ambush foragers. Although baseline TFRs appear phylogenetically stable in some lizard taxa, that is a consequence of concordant stability of foraging mode: when foraging mode shifts within taxa, so does baseline TFR. Also, baseline TFR is a good predictor of prey chemical discriminatory ability, as we established a strong positive relationship between baseline TFR and TFR in response to prey. Baseline TFR is unrelated to diet. Essentially, foraging mode, not phylogenetic relatedness, drives convergent evolution of similar levels of squamate chemosensory investigation.     

The role of character displacement in the molarization of hominin mandibular premolars

Closely related species are likely to experience resource competition in areas where their ranges overlap. Fossil evidence suggests that hominins in East Africa c. 2–1.5 million years ago may have lived synchronically and sympatrically, and that competition may have contributed to the different tooth sizes observed in Homo and Paranthropus. To assess the likelihood that these taxa overlapped, we applied a character displacement model to the postcanine tooth size of fossil hominins and validated this model in populations of living primates. Mandibular fourth premolar (P₄) crown size was measured from fossil taxa and from living primate species where dietary overlap is established. Dimensions of the P₄ crown were fitted to a character matrix and described as the response variables of a generalized linear model that took taxon and location as input variables. The model recovered significant divergence in samples of closely related, living primates. When applied to fossil hominins the same model detected strong indications of character displacement between early Homo and Paranthropus (P = 0.002) on the basis of their P₄ crown size. Our study is an example of how ecologically informed morphologies measured in appropriate extant referents can provide a comparative context for assessing community and ecological evolution in the fossil record.     

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.     

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.     

BODY SIZE DIVERSIFICATION IN ANOLIS: NOVEL ENVIRONMENT AND ISLAND EFFECTS

Extreme morphologies of many insular taxa suggest that islands have unusual properties that influence the tempo and mode of evolution. Yet whether insularity per se promotes rapid phenotypic evolution remains largely untested. We extend a phylogenetic comparative approach to test the influence of novel environments versus insularity on rates of body size and sexual size dimorphism diversification in Anolis . Rates of body size diversification among small-island and mainland species were similar to those of anole species on the Greater Antilles. However, the Greater Antilles taxa that colonized small islands and the mainland are ecologically nonrandom: rates of body size diversification among small-island and mainland species are high compared to their large-island sister taxa. Furthermore, rates of diversification in sexual size dimorphism on small islands are high compared to all large-island and mainland lineages. We suggest that elevated diversifying selection, particularly as a result of ecological release, may drive high rates of body size diversification in both small-island and mainland novel environments. In contrast, high abundance (prevalent among small-island lizard communities) mediating intraspecific resource competition and male–male competition may explain why sexual size dimorphism diversifies faster among small-island lineages than among their mainland and large-island relatives.     

Autoregressive models for estimating phylogenetic and environmental effects: accounting for within-species variations

Comparative methods are used to investigate the attributes of present species or higher taxa. Difficulties arise from the phylogenetic heritage: taxa are not independent and neglecting phylogenetic inertia can lead to inaccurate results. Within-species variations in life-history traits are also not negligible, but most comparative methods are not designed to take them into account. Taxa are generally described by a single value for each trait. We have developed a new model which permits the incorporation of both the phylogenetic relationships among populations and within-species variations. This is an extension of classical autoregressive models. This family of models was used to study the effect of fishing on six demographic traits measured on 77 populations of teleost fishes.