Bayesian estimation of ancestral character states on phylogenies

Biologists frequently attempt to infer the character states at ancestral nodes of a phylogeny from the distribution of traits observed in contemporary organisms. Because phylogenies are normally inferences from data, it is desirable to account for the uncertainty in estimates of the tree and its branch lengths when making inferences about ancestral states or other comparative parameters. Here we present a general Bayesian approach for testing comparative hypotheses across statistically justified samples of phylogenies, focusing on the specific issue of reconstructing ancestral states. The method uses Markov chain Monte Carlo techniques for sampling phylogenetic trees and for investigating the parameters of a statistical model of trait evolution. We describe how to combine information about the uncertainty of the phylogeny with uncertainty in the estimate of the ancestral state. Our approach does not constrain the sample of trees only to those that contain the ancestral node or nodes of interest, and we show how to reconstruct ancestral states of uncertain nodes using a most-recent-common-ancestor approach. We illustrate the methods with data on ribonuclease evolution in the Artiodactyla. Software implementing the methods (BayesMultiState) is available from the authors.     

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.     

Bayesian inference of character evolution

Much recent progress in evolutionary biology is based on the inference of ancestral states and past transformations in important traits on phylogenetic trees. These exercises often assume that the tree is known without error and that ancestral states and character change can be mapped onto it exactly. In reality, there is often considerable uncertainty about both the tree and the character mapping. Recently introduced Bayesian statistical methods enable the study of character evolution while simultaneously accounting for both phylogenetic and mapping uncertainty, adding much needed credibility to the reconstruction of evolutionary history.     

Reconstructing ancestral character states: a critical reappraisal

Using parsimony to reconstruct ancestral character states on a phylogenetic tree has become a popular method for testing ecological and evolutionary hypotheses. Despite its popularity, the assumptions and uncertainties of reconstructing the ancestral states of a single character have received less attention than the much less challenging endeavor of reconstructing phylogenetic trees from many characters. Recent research suggests that parsimony reconstructions are often sensitive to violations of the almost universal assumption of equal probabilities of gains and losses. In addition, maximum likelihood has been developed as an alternative to parsimony reconstruction, and has also revealed a surprising amount of uncertainty in ancestral reconstructions.     

Evolution of life history and behavior in Hominidae: Towards phylogenetic reconstruction of the chimpanzee–human last common ancestor

The origin of the fundamental behavioral differences between humans and our closest living relatives is one of the central issues of evolutionary anthropology. The prominent, chimpanzee-based referential model of early hominin behavior has recently been challenged on the basis of broad multispecies comparisons and newly discovered fossil evidence. Here, we argue that while behavioral data on extant great apes are extremely relevant for reconstruction of ancestral behaviors, these behaviors should be reconstructed trait by trait using formal phylogenetic methods. Using the widely accepted hominoid phylogenetic tree, we perform a series of character optimization analyses using 65 selected life-history and behavioral characters for all extant hominid species. This analysis allows us to reconstruct the character states of the last common ancestors of Hominoidea, Hominidae, and the chimpanzee–human last common ancestor. Our analyses demonstrate that many fundamental behavioral and life-history attributes of hominids (including humans) are evidently ancient and likely inherited from the common ancestor of all hominids. However, numerous behaviors present in extant great apes represent their own terminal autapomorphies (both uniquely derived and homoplastic). Any evolutionary model that uses a single extant species to explain behavioral evolution of early hominins is therefore of limited use. In contrast, phylogenetic reconstruction of ancestral states is able to provide a detailed suite of behavioral, ecological and life-history characters for each hypothetical ancestor. The living great apes therefore play an important role for the confident identification of the traits found in the chimpanzee–human last common ancestor, some of which are likely to represent behaviors of the fossil hominins.     

Something for nothing? Reconstruction of ancestral character states in asterinid sea star development

SUMMARY Traits from early development mapped onto phylogenetic trees can potentially offer insight into the evolutionary history of development by inferring the states of those characters among ancestors at nodes in the phylogeny. A key and often-overlooked aspect of such mapping is the underlying model of character evolution. Without a well-supported and realistic model ("nothing"), character mapping of ancestral traits onto phylogenetic trees might often return results ("something") that lack a sound basis. Here we reconsider a challenging case study in this area of evolutionary developmental biology: the inference of ancestral states for ecological and morphological characters in the reproduction and larval development of asterinid sea stars. We apply improved analytical methods to an expanded set of asterinid phylogenetic data and developmental character states. This analysis shows that the new methods might generally offer some independent insight into choice of a model of character evolution, but that in the specific case of asterinid sea stars the quantitative features of the model (especially the relative probabilities of different directions of change) have an important effect on the results. We suggest caution in applying ancestral state reconstructions in the absence of an independently corroborated model of character evolution, and highlight the need for such modeling in evolutionary developmental biology.     

Partially incorrect fossil data augment analyses of discrete trait evolution in living species

Ancestral state reconstruction of discrete character traits is often vital when attempting to understand the origins and homology of traits in living species. The addition of fossils has been shown to alter our understanding of trait evolution in extant taxa, but researchers may avoid using fossils alongside extant species if only few are known, or if the designation of the trait of interest is uncertain. Here, I investigate the impacts of fossils and incorrectly coded fossils in the ancestral state reconstruction of discrete morphological characters under a likelihood model. Under simulated phylogenies and data, likelihood-based models are generally accurate when estimating ancestral node values. Analyses with combined fossil and extant data always outperform analyses with extant species alone, even when around one quarter of the fossil information is incorrect. These results are especially pronounced when model assumptions are violated, such as when there is a trend away from the root value. Fossil data are of particular importance when attempting to estimate the root node character state. Attempts should be made to include fossils in analysis of discrete traits under likelihood, even if there is uncertainty in the fossil trait data.     

No substitute for real data: A cautionary note on the use of phylogenies from birth–death polytomy resolvers for downstream comparative analyses

The statistical estimation of phylogenies is always associated with uncertainty, and accommodating this uncertainty is an important component of modern phylogenetic comparative analysis. The birth–death polytomy resolver is a method of accounting for phylogenetic uncertainty that places missing (unsampled) taxa onto phylogenetic trees, using taxonomic information alone. Recent studies of birds and mammals have used this approach to generate pseudoposterior distributions of phylogenetic trees that are complete at the species level, even in the absence of genetic data for many species. Many researchers have used these distributions of phylogenies for downstream evolutionary analyses that involve inferences on phenotypic evolution, geography, and community assembly. I demonstrate that the use of phylogenies constructed in this fashion is inappropriate for many questions involving traits. Because species are placed on trees at random with respect to trait values, the birth–death polytomy resolver breaks down natural patterns of trait phylogenetic structure. Inferences based on these trees are predictably and often drastically biased in a direction that depends on the underlying (true) pattern of phylogenetic structure in traits. I illustrate the severity of the phenomenon for both continuous and discrete traits using examples from a global bird phylogeny.     

Behavioural evolution in penguins does not reflect phylogeny

Over the past two decades, behavioural biologists and ecologists have made effective use of the comparative method, but have often stopped short of adopting an explicitly phylogenetic approach. We examined 68 behaviour and life history (BLH) traits of 15 penguin species to: (i) infer penguin phylogeny, (ii) assess homology of behavioural characters, and (iii) evaluate hypotheses about character evolution and ancestral states. Parsimony analysis of the BLH dataset found either two shortest trees (characters coded as unordered) or a single shortest tree (characters coded as a combination of unordered and Dollo). The BLH data had significant structure. Kishino–Hasegawa tests indicated that BLH trees were significantly different from most previous estimates of penguin phylogeny. The BLH phylogeny generated from Dollo characters appeared to be less accurate than the tree derived from the completely unordered dataset. Dividing BLH data into display and non‐display traits resulted in no significant differences in level of homoplasy and no difference in the accuracy of phylogeny. Tests for homology of BLH traits were performed by mapping the characters onto a molecular tree. Assuming that independent gains are less likely than losses of character states, 65 of the 68 characters were likely to be homologous across taxa, and at least several characters appeared to have been stable since the origin of modern penguins around 30 Myr. Finally, the likely BLH traits of the most recent common ancestor of extant penguins were reconstructed from character states along the internal branch leading to the penguins. This analysis suggested that the “proto‐penguin” probably had a similar life history to current temperate penguins but few ritualized behaviours. A southern, cool‐temperate origin of penguins is suggested.     

Hunter-Gatherers and the Origins of Religion

Recent studies of the evolution of religion have revealed the cognitive underpinnings of belief in supernatural agents, the role of ritual in promoting cooperation, and the contribution of morally punishing high gods to the growth and stabilization of human society. The universality of religion across human society points to a deep evolutionary past. However, specific traits of nascent religiosity, and the sequence in which they emerged, have remained unknown. Here we reconstruct the evolution of religious beliefs and behaviors in early modern humans using a global sample of hunter-gatherers and seven traits describing hunter-gatherer religiosity: animism, belief in an afterlife, shamanism, ancestor worship, high gods, and worship of ancestors or high gods who are active in human affairs. We reconstruct ancestral character states using a time-calibrated supertree based on published phylogenetic trees and linguistic classification and then test for correlated evolution between the characters and for the direction of cultural change. Results indicate that the oldest trait of religion, present in the most recent common ancestor of present-day hunter-gatherers, was animism, in agreement with long-standing beliefs about the fundamental role of this trait. Belief in an afterlife emerged, followed by shamanism and ancestor worship. Ancestor spirits or high gods who are active in human affairs were absent in early humans, suggesting a deep history for the egalitarian nature of hunter-gatherer societies. There is a significant positive relationship between most characters investigated, but the trait “high gods” stands apart, suggesting that belief in a single creator deity can emerge in a society regardless of other aspects of its religion.     

CORRELATED EVOLUTION OF MIGRATION AND SEXUAL DICHROMATISM IN THE NEW WORLD ORIOLES (ICTERUS)

The evolution of sexual dimorphism has long been attributed to sexual selection, specifically as it would drive repeated gains of elaborate male traits. In contrast to this pattern, New World oriole species all exhibit elaborate male plumage, and the repeated gains of sexual dichromatism observed in the genus are due to losses of female elaboration. Interestingly, most sexually dichromatic orioles belong to migratory or temperate‐breeding clades. Using character scoring and ancestral state reconstructions from two recent studies in Icterus, we tested a hypothesis of correlated evolution between migration and sexual dichromatism. We employed two discrete phylogenetic comparative approaches: the concentrated changes test and Pagel's discrete likelihood test. Our results show that the evolution of these traits is significantly correlated (CCT: uncorrected P < 0.05; ML: LRT = 12.470, P < 0.005). Indeed, our best model of character evolution suggests that gains of sexual dichromatism are 23 times more likely to occur in migratory taxa. This study demonstrates that a life‐history trait with no direct relationship with sexual selection has a strong influence on the evolution of sexual dichromatism. We recommend that researchers further investigate the role of selection on elaborate female traits in the evolution of sexual dimorphism.     

The phylogeny of a species-level tendency: species heritability and possible deep origins of Bergmann's rule in tetrapods

One of the most widely recognized generalizations in biology is Bergmann's rule, the observation that, within species of birds and mammals, body size tends to be inversely related to ambient temperature. Recent studies indicate that turtles and salamanders also tend to follow Bergmann's rule, which hints that this species-level tendency originated early in tetrapod history. Furthermore, exceptions to Bergmann's rule are concentrated within squamate reptiles (lizards and snakes), suggesting that the tendency to express a Bergmann's rule cline may be heritable at the species level. We evaluated species-level heritability and early origination of Bergmann's rule by mapping size-latitude relationships for 352 species onto a tetrapod phylogeny. When the largest available dataset is used, Bergmann's rule shows significant phylogenetic signal, indicating species-level heritability. This represents one of the few demonstrations of heritability for an emergent species-level property and the first for an ecogeographic rule. When species are discretely coded as showing either Bergmann's rule or its converse, parsimony reconstructions suggest that: (1) the tendency to follow Bergmann's rule is ancestral for tetrapods, and (2) most extant species that express the rule have retained this tendency from that ancient ancestor. The first inference also generally holds when the discrete data or size-latitude correlation coefficients are analyzed using maximum likelihood, although the results are only statistically significant for some versions of the discrete analyses. The best estimates of ancestral states suggest that the traditional adaptive explanation for Bergmann's rule-conservation of metabolic heat-was not involved in the origin of the trait since that origin predates the evolution of endothermy. A more general thermoregulatory hypothesis could apply to endotherms and some ectotherms, but fails to explain why salamanders have retained Bergmann's rule. Thus, if thermoregulation underlies the origin of a Bergmann's rule tendency, this trait may have been continuously maintained while its cause changed. Alternatively, thermoregulation may not underlie Bergmann's rule in any tetrapod group. The results also suggest that many extinct groups not included in our analyses followed Bergmann's rule.     

Inferring the ancestral sexuality and reproductive condition in sponges (Porifera)

Considerable diversity abounds among sponges with respect to reproductive and developmental biology. Their ancestral sexual mode (gonochorism vs. hermaphroditism) and reproductive condition (oviparity vs. viviparity) however remain unclear, and these traits appear to have undergone correlated evolution in the phylum. To infer ancestral traits and investigate this putative correlation, we used DNA sequence data from two loci (18S ribosomal RNA and cytochrome c oxidase subunit I) to explore the phylogenetic relationships of 62 sponges whose reproductive traits have been previously documented. Although the inferred tree topologies, using the limited data available, favoured paraphyly of sponges, we also investigated ancestral character‐state reconstruction on a phylogeny with constrained sponge monophyly. Both parsimony‐ and likelihood‐based ancestral state reconstructions indicate that viviparity (brooding) was the likely reproductive mode of the ancestral sponge. Hermaphroditism is favoured over gonochorism as the sexual condition of the sponge ancestor under parsimony, but the reconstruction is ambiguous under likelihood, rendering the ancestry of sexuality unresolved in our study. These results are insensitive to the constraint of sponge monophyly when tracing the reproductive characters using parsimony methods. However, the maximum likelihood analysis of the monophyletic hypothetical tree rendered gonochorism as ancestral for the phylum. A test of trait correlation unambiguously favours the concerted evolution of sexuality and reproductive mode in sponges (hermaphroditism/viviparity, gonochorism/oviparity). Although testing ecological hypotheses for the pattern of sponge reproduction is beyond the scope of our analyses, we postulate that certain physiological constrains might be key causes for the correlation of reproductive characters.     

Reconstructing ancestral ecologies: challenges and possible solutions

There are several ways to extract information about the evolutionary ecology of clades from their phylogenies. Of these, character state optimization and 'ancestor reconstruction' are perhaps the most widely used despite their being fraught with assumptions and potential pitfalls. Requirements for robust inferences of ancestral traits in general (i.e. those applicable to all types of characters) include accurate and robust phylogenetic hypotheses, complete species-level sampling and the appropriate choice of optimality criterion. Ecological characters, however, also require careful consideration of methods for accounting for intraspecific variability. Such methods include 'Presence Coding' and 'Polymorphism Coding' for discrete ecological characters, and 'Range Coding' and 'MaxMin Coding' for continuously variable characters. Ultimately, however, historical inferences such as these are, as with phylogenetic inference itself, associated with a degree of uncertainty. Statistically based uncertainty estimates are available within the context of model-based inference (e.g. maximum likelihood and Bayesian); however, these measures are only as reliable as the chosen model is appropriate. Although generally thought to preclude the possibility of measuring relative uncertainty or support for alternative possible reconstructions, certain useful non-statistical support measures (i.e. 'Sharkey support' and 'Parsimony support') are applicable to parsimony reconstructions.     

Mitochondrial DNA as a tool for reconstructing past life‐history traits in mammals

Reconstructing the ancestral characteristics of species is a major goal in evolutionary and comparative biology. Unfortunately, fossils are not always available and sufficiently informative, and phylogenetic methods based on models of character evolution can be unsatisfactory. Genomic data offer a new opportunity to estimate ancestral character states, through (i) the correlation between DNA evolutionary processes and species life‐history traits and (ii) available reliable methods for ancestral sequence inference. Here, we assess the relevance of mitochondrial DNA – the most popular molecular marker in animals – as a predictor of ancestral life‐history traits in mammals, using the order of Cetartiodactyla as a benchmark. Using the complete set of 13 mitochondrial protein‐coding genes, we show that the lineage‐specific nonsynonymous over synonymous substitution rate ratio (dN/dS) is closely correlated with the species body mass, longevity and age of sexual maturity in Cetartiodactyla and can be used as a marker of ancestral traits provided that the noise introduced by short branches is appropriately dealt with. Based on ancestral dN/dS estimates, we predict that the first cetartiodactyls were relatively small animals (around 20 kg). This finding is in accordance with Cope's rule and the fossil record but could not be recovered via continuous character evolution methods.     

Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model

Violation of the molecular clock has been amply documented, and is now routinely taken into account by molecular dating methods. Comparative analyses have revealed a systematic component in rate variation, relating it to the evolution of life-history traits, such as body size or generation time. Life-history evolution can be reconstructed using Brownian models. However, the resulting estimates are typically uncertain, and potentially sensitive to the underlying assumptions. As a way of obtaining more accurate ancestral trait and divergence time reconstructions, correlations between life-history traits and substitution rates could be used as an additional source of information. In this direction, a Bayesian framework for jointly reconstructing rates, traits, and dates was previously introduced. Here, we apply this model to a 17 protein-coding gene alignment for 73 placental taxa. Our analysis indicates that the coupling between molecules and life history can lead to a reevaluation of ancestral life-history profiles, in particular for groups displaying convergent evolution in body size. However, reconstructions are sensitive to fossil calibrations and to the Brownian assumption. Altogether, our analysis suggests that further integrating inference of rates and traits might be particularly useful for neontological macroevolutionary comparative studies.     

Independent contrasts succeed where ancestor reconstruction fails in a known bacteriophage phylogeny

Abstract.— Methods of ancestor reconstruction are important tools for evolutionary inference that are difficult to test empirically because ancestral states are rarely known with certainty. We evaluated reconstruction methods for continuous phenotypic characters using taxa from an experimentally generated bacteriophage phylogeny. Except for one slowly evolving character, the estimated ancestral states of continuous phenotypic characters were highly inaccurate and biased, even when including a known ancestor at the root. This error was caused by a directional trend in character evolution and by rapid rates of character evolution. Computer simulations confirmed that such factors affect reconstruction of continuous characters in general. We also used phenotypic viral characters to evaluate two methods that attempt to estimate the correlation between characters during evolution. Whereas a nonphylogenetic regression was relatively inaccurate and biased, independent contrasts accurately estimated the correlation between characters with little bias.     

Understanding Phenotypical Character Evolution in Parmelioid Lichenized Fungi (Parmeliaceae,Ascomycota)

Parmelioid lichens form a species-rich group of predominantly foliose and fruticose lichenized fungi encompassing a broad range of morphological and chemical diversity. Using a multilocus approach, we reconstructed a phylogeny including 323 OTUs of parmelioid lichens and employed ancestral character reconstruction methods to understand the phenotypical evolution within this speciose group of lichen-forming fungi. Specifically, we were interested in the evolution of growth form, epicortex structure, and cortical chemistry. Since previous studies have shown that results may differ depending on the reconstruction method used, here we employed both maximum-parsimony and maximum-likelihood approaches to reconstruct ancestral character states. We have also implemented binary and multistate coding of characters and performed parallel analyses with both coding types to assess for potential coding-based biases. We reconstructed the ancestral states for nine well-supported major clades in the parmelioid group, two higher-level sister groups and the ancestral character state for all parmelioid lichens. We found that different methods for coding phenotypical characters and different ancestral character state reconstruction methods mostly resulted in identical reconstructions but yield conflicting inferences of ancestral states, in some cases. However, we found support for the ancestor of parmelioid lichens having been a foliose lichen with a non-pored epicortex and pseudocyphellae. Our data suggest that some traits exhibit patterns of evolution consistent with adaptive radiation.     

Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis

In historical biogeography, model-based inference methods for reconstructing the evolution of geographic ranges on phylogenetic trees are poorly developed relative to the diversity of analogous methods available for inferring character evolution. We attempt to rectify this deficiency by constructing a dispersal-extinction-cladogenesis (DEC) model for geographic range evolution that specifies instantaneous transition rates between discrete states (ranges) along phylogenetic branches and apply it to estimating likelihoods of ancestral states (range inheritance scenarios) at cladogenesis events. Unlike an earlier version of this approach, the present model allows for an analytical solution to probabilities of range transitions as a function of time, enabling free parameters in the model, rates of dispersal, and local extinction to be estimated by maximum likelihood. Simulation results indicate that accurate parameter estimates may be difficult to obtain in practice but also show that ancestral range inheritance scenarios nevertheless can be correctly recovered with high success if rates of range evolution are low relative to the rate of cladogenesis. We apply the DEC model to a previously published, exemplary case study of island biogeography involving Hawaiian endemic angiosperms in Psychotria (Rubiaceae), showing how the DEC model can be iteratively refined from inspecting inferences of range evolution and also how geological constraints involving times of island origin may be imposed on the likelihood function. The DEC model is sufficiently similar to character models that it might serve as a gateway through which many existing comparative methods for characters could be imported into the realm of historical biogeography; moreover, it might also inspire the conceptual expansion of character models toward inclusion of evolutionary change as directly coincident, either as cause or consequence, with cladogenesis events. The DEC model is thus an incremental advance that highlights considerable potential in the nascent field of model-based historical biogeographic inference.     

Contrasting phylogenetic signals and evolutionary rates in floral traits of Neotropical lianas

The diversity of floral forms has long been considered a prime example of radiation through natural selection. However, little is still known about the evolution of floral traits, a critical piece of evidence for the understanding of the processes that may have driven flower evolution. We studied the pattern of evolution of quantitative floral traits in a group of Neotropical lianas (Bignonieae, Bignoniaceae) and used a time‐calibrated phylogeny as basis to: (1) test for phylogenetic signal in 16 continuous floral traits; (2) evaluate the rate of evolution in those traits; and (3) reconstruct the ancestral state of the individual traits. Variation in floral traits among extant species of Bignonieae was highly explained by their phylogenetic history. However, opposite signals were found in floral traits associated with the attraction of pollinators (calyx and corolla) and pollen transfer (androecium and gynoecium), suggesting a differential role of selection in different floral whorls. Phylogenetic independent contrasts indicate that traits evolved at different rates, whereas ancestral character state reconstructions indicate that the ancestral size of most flower traits was larger than the mean observed sizes of the same traits in extant species. The implications of these patterns for the reproductive biology of Bignonieae are discussed. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 378–390.