Fifty years of character compatibility concepts at work

In the mid 19th century,systematic biologists realized that observable similarities and differences among a group of related species could be the basis for hypotheses about the evolutionary relationships among the species and their ancestors.Such hypotheses Can be expressed as characters.A character is comprised of two or more character states of species considered to be similar with respect to a basis for comparison.The states of a character may also be arranged into a character state tree to hypothesize speciation events associated with changes from one character state to another.In the mid 20th century.some systematists realized that sometimes paxrs of characters(or character state trees)could be incompatible as hypotheses,i.e.,they could not both be true.Through the 1950s,'60s and'70s,tests for,and ways to resolve,incompatibilities were used to estimate an ancestor relation based on mutually compatible characters.An estimate was often shown as a diagram connecting ancestors to their immediate descendants(not quite correctly)called a phylogenetic tree.More recently,other applications of compatibility concepts have been developed,including:identify characters that appear to be random in the context of their data set;combine estimates of ancestor relations for subsets of taxa in a larger collection into a single estimate(a so-called supertree)for the whole collection;and interpret geographic patterns in an evolutionary context.     

Perils of paralogy: using HSP70 genes for inferring organismal phylogenies

Conserved genes have found their way into the mainstream of molecular systematics. Many of these genes are members of multigene families. A difficulty with using single genes of multigene families for phylogenetic inference is that genes from one species may be paralogous to those from another taxon. We focus attention on this problem using heat shock 70 (HSP70) genes. Using polymerase chain reaction techniques with genomic DNA, we isolated and sequenced 123 distinct sequences from 12 species of sharks. Phylogenetic analysis indicated that the sequences cluster with constituitively expressed cytoplasmic heat shock-like genes. Three highly divergent gene clades were sampled. A number of similar sequences were sampled from each species within each distinct gene clade. Comparison of published species trees with an HSP70 gene tree inferred using Bayesian phylogenetic analysis revealed several cases of gene duplication and differential sorting of gene lineages within this group of sharks. Gene tree parsimony based on the objective criteria of duplication and losses showed that previously published hypotheses of species relationships and two novel hypothesis based on Bayesian phylogenetics were concordant with the history of HSP70 gene duplication and loss. By contrast, two published hypotheses based on morphological data were not significantly different from the null hypothesis of a random association between species relatedness and the HSP70 gene tree. These results suggest that gene tree parsimony using data from multigene families can be used for inferring species relationships or testing published alternative hypotheses. More importantly, the results suggest that systematic studies relying on phylogenetic inferences from HSP70 genes may by plagued by unrecognized paralogy of sampled genes. Our results underscore the distinction between gene and species trees and highlight an underappreciated source of discordance between gene trees and organismal phylogeny, i.e., unrecognized paralogy of sampled genes.     

Species tree estimation for the late blight pathogen, Phytophthora infestans, and close relatives

To better understand the evolutionary history of a group of organisms, an accurate estimate of the species phylogeny must be known. Traditionally, gene trees have served as a proxy for the species tree, although it was acknowledged early on that these trees represented different evolutionary processes. Discordances among gene trees and between the gene trees and the species tree are also expected in closely related species that have rapidly diverged, due to processes such as the incomplete sorting of ancestral polymorphisms. Recently, methods have been developed for the explicit estimation of species trees, using information from multilocus gene trees while accommodating heterogeneity among them. Here we have used three distinct approaches to estimate the species tree for five Phytophthora pathogens, including P. infestans, the causal agent of late blight disease in potato and tomato. Our concatenation-based "supergene" approach was unable to resolve relationships even with data from both the nuclear and mitochondrial genomes, and from multiple isolates per species. Our multispecies coalescent approach using both Bayesian and maximum likelihood methods was able to estimate a moderately supported species tree showing a close relationship among P. infestans, P. andina, and P. ipomoeae. The topology of the species tree was also identical to the dominant phylogenetic history estimated in our third approach, Bayesian concordance analysis. Our results support previous suggestions that P. andina is a hybrid species, with P. infestans representing one parental lineage. The other parental lineage is not known, but represents an independent evolutionary lineage more closely related to P. ipomoeae. While all five species likely originated in the New World, further study is needed to determine when and under what conditions this hybridization event may have occurred.     

To tree or not to tree

The practice of tracking geographical divergence along a phylogenetic tree has added an evolutionary perspective to biogeographic analysis within single species. In spite of the popularity of phylogeography, there is an emerging problem. Recurrent mutation and recombination both create homoplasy, multiple evolutionary occurrences of the same character that are identical in state but not identical by descent. Homoplasic molecular data are phylogenetically ambiguous. Converting homoplasic molecular data into a tree represents an extrapolation, and there can be myriad candidate trees among which to choose. Derivative biogeographic analyses of 'the tree' are analyses of that extrapolation, and the results depend on the tree chosen. I explore the informational aspects of converting a multicharacter data set into a phylogenetic tree, and then explore what happens when that tree is used for population analysis. Three conclusions follow: (i) some trees are better than others; good trees are true to the data, whereas bad trees are not; (ii) for biogeographic analysis, we should use only good trees, which yield the same biogeographic inference as the phenetic data, but little more; and (iii) the reliable biogeographic inference is inherent in the phenetic data, not the trees.     

Gene trees, species trees, and morphology converge on a similar phylogeny of living gars (Actinopterygii: Holostei: Lepisosteidae), an ancient clade of ray-finned fishes

Extant gars represent the remaining members of a formerly diverse assemblage of ancient ray-finned fishes and have been the subject of multiple phylogenetic analyses using morphological data. Here, we present the first hypothesis of phylogenetic relationships among living gar species based on molecular data, through the examination of gene tree heterogeneity and coalescent species tree analyses of a portion of one mitochondrial (COI) and seven nuclear (ENC1, myh6, plagl2, S7 ribosomal protein intron 1, sreb2, tbr1, and zic1) genes. Individual gene trees displayed varying degrees of resolution with regards to species-level relationships, and the gene trees inferred from COI and the S7 intron were the only two that were completely resolved. Coalescent species tree analyses of nuclear genes resulted in a well-resolved and strongly supported phylogenetic tree of living gar species, for which Bayesian posterior node support was further improved by the inclusion of the mitochondrial gene. Species-level relationships among gars inferred from our molecular data set were highly congruent with previously published morphological phylogenies, with the exception of the placement of two species, Lepisosteus osseus and L. platostomus. Re-examination of the character coding used by previous authors provided partial resolution of this topological discordance, resulting in broad concordance in the phylogenies inferred from individual genes, the coalescent species tree analysis, and morphology. The completely resolved phylogeny inferred from the molecular data set with strong Bayesian posterior support at all nodes provided insights into the potential for introgressive hybridization and patterns of allopatric speciation in the evolutionary history of living gars, as well as a solid foundation for future examinations of functional diversification and evolutionary stasis in a "living fossil" lineage.     

Phylogenomic assessment of the role of hybridization and introgression in trait evolution

Trait evolution among a set of species—a central theme in evolutionary biology—has long been understood and analyzed with respect to a species tree. However, the field of phylogenomics, which has been propelled by advances in sequencing technologies, has ushered in the era of species/gene tree incongruence and, consequently, a more nuanced understanding of trait evolution. For a trait whose states are incongruent with the branching patterns in the species tree, the same state could have arisen independently in different species (homoplasy) or followed the branching patterns of gene trees, incongruent with the species tree (hemiplasy). Another evolutionary process whose extent and significance are better revealed by phylogenomic studies is gene flow between different species. In this work, we present a phylogenomic method for assessing the role of hybridization and introgression in the evolution of polymorphic or monomorphic binary traits. We apply the method to simulated evolutionary scenarios to demonstrate the interplay between the parameters of the evolutionary history and the role of introgression in a binary trait’s evolution (which we call xenoplasy). Very importantly, we demonstrate, including on a biological data set, that inferring a species tree and using it for trait evolution analysis in the presence of gene flow could lead to misleading hypotheses about trait evolution.     

A consensus tree approach for reconstructing human evolutionary history and detecting population substructure

The random accumulation of variations in the human genome over time implicitly encodes a history of how human populations have arisen, dispersed, and intermixed since we emerged as a species. Reconstructing that history is a challenging computational and statistical problem but has important applications both to basic research and to the discovery of genotype-phenotype correlations. We present a novel approach to inferring human evolutionary history from genetic variation data. We use the idea of consensus trees, a technique generally used to reconcile species trees from divergent gene trees, adapting it to the problem of finding robust relationships within a set of intraspecies phylogenies derived from local regions of the genome. Validation on both simulated and real data shows the method to be effective in recapitulating known true structure of the data closely matching our best current understanding of human evolutionary history. Additional comparison with results of leading methods for the problem of population substructure assignment verifies that our method provides comparable accuracy in identifying meaningful population subgroups in addition to inferring relationships among them. The consensus tree approach thus provides a promising new model for the robust inference of substructure and ancestry from large-scale genetic variation data.     

Reconciling gene and genome duplication events: using multiple nuclear gene families to infer the phylogeny of the aquatic plant family Pontederiaceae

Most plant phylogenetic inference has used DNA sequence data from the plastid genome. This genome represents a single genealogical sample with no recombination among genes, potentially limiting the resolution of evolutionary relationships in some contexts. In contrast, nuclear DNA is inherently more difficult to employ for phylogeny reconstruction because major mutational events in the genome, including polyploidization, gene duplication, and gene extinction can result in homologous gene copies that are difficult to identify as orthologs or paralogs. Gene tree parsimony (GTP) can be used to infer the rooted species tree by fitting gene genealogies to species trees while simultaneously minimizing the estimated number of duplications needed to reconcile conflicts among them. Here, we use GTP for five nuclear gene families and a previously published plastid data set to reconstruct the phylogenetic backbone of the aquatic plant family Pontederiaceae. Plastid-based phylogenetic studies strongly supported extensive paraphyly of Eichhornia (one of the four major genera) but also depicted considerable ambiguity concerning the true root placement for the family. Our results indicate that species trees inferred from the nuclear genes (alone and in combination with the plastid data) are highly congruent with gene trees inferred from plastid data alone. Consideration of optimal and suboptimal gene tree reconciliations place the root of the family at (or near) a branch leading to the rare and locally restricted E. meyeri. We also explore methods to incorporate uncertainty in individual gene trees during reconciliation by considering their individual bootstrap profiles and relate inferred excesses of gene duplication events on individual branches to whole-genome duplication events inferred for the same branches. Our study improves understanding of the phylogenetic history of Pontederiaceae and also demonstrates the utility of GTP for phylogenetic analysis.     

PARSIMONY AND THE CHOICE BETWEEN DIFFERENT TRANSFORMATIONS FOR THE SAME CHARACTER SET

Abstract— When phylogeneticists choose among alternative hypotheses, they choose the one that requires the fewest ad hoc assumptions, i.e. the one that is the most parsimonious. For some systematists, choosing among alternative transformation series for the same set of taxa is equivalent to attaining trees with shorter length and minimal homoplasy. Homoplasy is shown to be composed of hierarchical discordance and scattering, which are recognized and described for the first time. Neither the consistency nor retention indices can be used in assessing different theories of multistate character transformation because both are affected by the shape of the transformation series rather than the character state distribution on a tree. Fits of transformations to a tree are better assessed by comparing the transformation to the cladogram character and the nearest neighbor network. Nearest neighbor networks are graphical representations of the nearest neighbor matrix. Transformations with the closest greatest number of matches between cladogram characters and the least complexity in the nearest neighbor network are preferred. These transformations are shown to make the fewest number of ad hoc statements and hence to be the most parsimonious. A means for obtaining cladogram characters and nearest neighbor matrices using a widely distributed microcomputer program is presented.     

Estimating species trees using approximate Bayesian computation

Development of methods for estimating species trees from multilocus data is a current challenge in evolutionary biology. We propose a method for estimating the species tree topology and branch lengths using approximate Bayesian computation (ABC). The method takes as data a sample of observed rooted gene tree topologies, and then iterates through the following sequence of steps: First, a randomly selected species tree is used to compute the distribution of rooted gene tree topologies. This distribution is then compared to the observed gene topology frequencies, and if the fit between the observed and the predicted distributions is close enough, the proposed species tree is retained. Repeating this many times leads to a collection of retained species trees that are then used to form the estimate of the overall species tree. We test the performance of the method, which we call ST-ABC, using both simulated and empirical data. The simulation study examines both symmetric and asymmetric species trees over a range of branch lengths and sample sizes. The results from the simulation study show that the model performs very well, giving accurate estimates for both the topology and the branch lengths across the conditions studied, and that a sample size of 25 loci appears to be adequate for the method. Further, we apply the method to two empirical cases: a 4-taxon data set for primates and a 7-taxon data set for yeast. In both cases, we find that estimates obtained with ST-ABC agree with previous studies. The method provides efficient estimation of the species tree, and does not require sequence data, but rather the observed distribution of rooted gene topologies without branch lengths. Therefore, this method is a useful alternative to other currently available methods for species tree estimation.     

Using phylogeographic analyses of gene trees to test species status and processes

A gene tree is an evolutionary reconstruction of the genealogical history of the genetic variation found in a sample of homologous genes or DNA regions that have experienced little or no recombination. Gene trees have the potential of straddling the interface between intra- and interspecific evolution. It is precisely at this interface that the process of speciation occurs, and gene trees can therefore be used as a powerful tool to probe this interface. One application is to infer species status. The cohesion species is defined as an evolutionary lineage or set of lineages with genetic exchangeability and/or ecological interchangeability. This species concept can be phrased in terms of null hypotheses that can be tested rigorously and objectively by using gene trees. First, an overlay of geography upon the gene tree is used to test the null hypothesis that the sample is from a single evolutionary lineage. This phase of testing can indicate that the sampled organisms are indeed from a single lineage and therefore a single cohesion species. In other cases, this null hypothesis is not rejected due to a lack of power or inadequate sampling. Alternatively, this null hypothesis can be rejected because two or more lineages are in the sample. The test can identify lineages even when hybridization and lineage sorting occur. Only when this null hypothesis is rejected is there the potential for more than one cohesion species. Although all cohesion species are evolutionary lineages, not all evolutionary lineages are cohesion species. Therefore, if the first null hypothesis is rejected, a second null hypothesis is tested that all lineages are genetically exchangeable and/or ecologically interchangeable. This second test is accomplished by direct contrasts of previously identified lineages or by overlaying reproductive and/or ecological data upon the gene tree and testing for significant transitions that are concordant with the previously identified lineages. Only when this second null hypothesis is rejected is a lineage elevated to the status of cohesion species. By using gene trees in this manner, species can be identified with objective, a priori criteria with an inference procedure that automatically yields much insight into the process of speciation. When one or more of the null hypotheses cannot be rejected, this procedure also provides specific guidance for future work that will be needed to judge species status.     

MEASURING EVOLUTIONARY CONSTRAINTS: A MARKOV MODEL FOR PHYLOGENETIC TRANSITIONS AMONG SEED DISPERSAL SYNDROMES

I introduce a Markov probabilistic model of transitions among discrete morphological states as a method for describing and testing nonrandom patterns of evolutionary change. The Markov model assumes one-generational dependency, i.e., that the future direction of evolutionary change depends on the current morphology of a species, not on any history of changes. This model is very flexible, allowing for any number of discrete states to describe morphology, yet permit rigorous testing of even complex evolutionary hypotheses. I apply this model to changes in seed dispersal mechanisms within 571 genera of Neotropical plants, using cladistic methods to infer the ancestral and derived states within each genus. I then test a series of progressively more complex hypotheses about the constraints that might shape the patterns of observed evolutionary transitions: 1) no transition constraints; 2) all dispersal mechanisms are equally labile evolutionarily; 3) the probability of particular evolutionary transitions among dispersal mechanisms depends on the descendant state but not on the ancestral state; 4) transition probabilities differ among pairs of dispersal mechanisms, but are reciprocal within such pairs. More complex hypotheses matched the data significantly better than did simpler hypotheses. However, only one of the hypotheses (reciprocal transitions) fit the observed data and then only for the most cautious interpretation of the frequencies of transitions within genera. These results suggest that evolutionary transitions among major adaptive syndromes are indeed ordered, and the observed patterns of transitions suggest possible reasons for such macroevolutionary structure.     

GeneTRACE-reconstruction of gene content of ancestral species

While current computational methods allow the reconstruction of individual ancestral protein sequences, reconstruction of complete gene content of ancestral species is not yet an established task. In this paper, we describe GENETRACE, an efficient linear-time algorithm that allows the reconstruction of evolutionary history of individual protein families as well as the complete gene content of ancestral species. The performance of the method was validated with a simulated evolution program called SimulEv. Our results indicate that given a set of correct phylogenetic profiles and a correct species tree, ancestral gene content can be reconstructed with sensitivity and selectivity of more than 90%. SimulEv simulations were also used to evaluate performance of the reconstruction of gene content-based phylogenetic trees, suggesting that these trees may be accurate at the terminal branches but suffer from long branch attraction near the root of the tree.     

iGTP: A software package for large-scale gene tree parsimony analysis

Background  

The ever-increasing wealth of genomic sequence information provides an unprecedented opportunity for large-scale phylogenetic analysis. However, species phylogeny inference is obfuscated by incongruence among gene trees due to evolutionary events such as gene duplication and loss, incomplete lineage sorting (deep coalescence), and horizontal gene transfer. Gene tree parsimony (GTP) addresses this issue by seeking a species tree that requires the minimum number of evolutionary events to reconcile a given set of incongruent gene trees. Despite its promise, the use of gene tree parsimony has been limited by the fact that existing software is either not fast enough to tackle large data sets or is restricted in the range of evolutionary events it can handle.     

From null community to non-randomly structured actual plant assemblages: parsimony analysis of species co-occurrences

Null community is a spatio‐temporal abstraction of an initial regional species pool from which local species pools and actual community assemblages are organized. Any process that causes joint responses of species with similar susceptibilities affects community assembly. Through time, sequential assembly processes change the composition of a species pool in a way analogous to the one in which evolutionary processes promote character changes from an ancestor to current species. The segregation of species occurrences in an actual community suggests that assembly processes non‐randomly structured the observed community assemblages. However, going backwards to imply the causes of a particular arrangement of species is a non‐trivial challenge. I merge these premises with the philosophical and methodological foundations of cladistics. I propound parsimony analysis of species co‐occurrences as an outstanding means of devising operational hypotheses about the assembly of any non‐randomly structured set of actual community assemblages related to a common species pool. To explore this approach, I used field data gathered in a suite of 10 wetland assemblages. First, I tested independence of 101 plant species occurrences by a null model. As significant non‐random species co‐occurrence was detected, I applied a parsimony analysis taking the species occurrences as attributes, the assemblages as terminal units, and a putative null community constituted by all the present local species as the root of the assembly suite. The analysis produced four most parsimonious trees of assembly relationships. These trees maximize the number of similarities among community assemblages that can be explained by the sole fact of sharing a common regional species pool. One most parsimonious spatio‐temporal arrangement of species occurrence changes was reconstructed on one of the trees. I interpret this reconstruction in terms of assembly events, species exclusions and recruitments, showing the potentialities of this analysis to formulate operational hypotheses about community organization.     

Genome-scale phylogenetics: inferring the plant tree of life from 18,896 gene trees

Phylogenetic analyses using genome-scale data sets must confront incongruence among gene trees, which in plants is exacerbated by frequent gene duplications and losses. Gene tree parsimony (GTP) is a phylogenetic optimization criterion in which a species tree that minimizes the number of gene duplications induced among a set of gene trees is selected. The run time performance of previous implementations has limited its use on large-scale data sets. We used new software that incorporates recent algorithmic advances to examine the performance of GTP on a plant data set consisting of 18,896 gene trees containing 510,922 protein sequences from 136 plant taxa (giving a combined alignment length of >2.9 million characters). The relationships inferred from the GTP analysis were largely consistent with previous large-scale studies of backbone plant phylogeny and resolved some controversial nodes. The placement of taxa that were present in few gene trees generally varied the most among GTP bootstrap replicates. Excluding these taxa either before or after the GTP analysis revealed high levels of phylogenetic support across plants. The analyses supported magnoliids sister to a eudicot + monocot clade and did not support the eurosid I and II clades. This study presents a nuclear genomic perspective on the broad-scale phylogenic relationships among plants, and it demonstrates that nuclear genes with a history of duplication and loss can be phylogenetically informative for resolving the plant tree of life.     

Phylogenetic analysis of RAD‐seq data: examining the influence of gene genealogy conflict on analysis of concatenated data

One of the major issues in phylogenetic analysis is that gene genealogies from different gene regions may not reflect the true species tree or history of speciation. This has led to considerable debate about whether concatenation of loci is the best approach for phylogenetic analysis. The application of Next‐generation sequencing techniques such as RAD‐seq generates thousands of relatively short sequence reads from across the genomes of the sampled taxa. These data sets are typically concatenated for phylogenetic analysis leading to data sets that contain millions of base pairs per taxon. The influence of gene region conflict among so many loci in determining the phylogenetic relationships among taxa is unclear. We simulated RAD‐seq data by sampling 100 and 500 base pairs from alignments of over 6000 coding regions that each produce one of three highly supported alternative phylogenies of seven species of Drosophila. We conducted phylogenetic analyses on different sets of these regions to vary the sampling of loci with alternative gene trees to examine the effect on detecting the species tree. Irrespective of sequence length sampled per region and which subset of regions was used, phylogenetic analyses of the concatenated data always recovered the species tree. The results suggest that concatenated alignments of Next‐generation data that consist of many short sequences are robust to gene tree/species tree conflict when the goal is to determine the phylogenetic relationships among taxa.     

Evolutionary stasis, constraint and other terminology describing evolutionary patterns

Current use of terms to describe evolutionary patterns is vague and inconsistent. In this paper, logical definitions of terms that describe specific evolutionary patterns are proposed. Evolutionary inertia is defined in a manner analogous to inertia in physics. A character in a static state of evolutionary inertia represents evolutionary stasis while a character showing consistent directional evolutionary change represents evolutionary thrust. I argue that evolutionary stasis should serve as the null hypothesis in all character evolution studies. Deviations from this null model consistent with alternative hypotheses (e.g. random drift, adaptation) can then give us insight into evolutionary processes. Failure to reject a null hypothesis of evolutionary stasis should not be used as a serious explanation of data. The term evolutionary constraint is appropriate only when a selective advantage for a character state transition is established but this transition is prevented by specific, identified factors. One type of evolutionary constraint discussed is evolutionary momentum. A final pattern of evolutionary change discussed is closely related to evolutionary thrust and is referred to as evolutionary acceleration. I provide examples of how this set of definitions can improve our ability to communicate interpretations of evolutionary patterns.     

Gene tree parsimony of multilocus snake venom protein families reveals species tree conflict as a result of multiple parallel gene loss

The proliferation of gene data from multiple loci of large multigene families has been greatly facilitated by considerable recent advances in sequence generation. The evolution of such gene families, which often undergo complex histories and different rates of change, combined with increases in sequence data, pose complex problems for traditional phylogenetic analyses, and in particular, those that aim to successfully recover species relationships from gene trees. Here, we implement gene tree parsimony analyses on multicopy gene family data sets of snake venom proteins for two separate groups of taxa, incorporating Bayesian posterior distributions as a rigorous strategy to account for the uncertainty present in gene trees. Gene tree parsimony largely failed to infer species trees congruent with each other or with species phylogenies derived from mitochondrial and single-copy nuclear sequences. Analysis of four toxin gene families from a large expressed sequence tag data set from the viper genus Echis failed to produce a consistent topology, and reanalysis of a previously published gene tree parsimony data set, from the family Elapidae, suggested that species tree topologies were predominantly unsupported. We suggest that gene tree parsimony failure in the family Elapidae is likely the result of unequal and/or incomplete sampling of paralogous genes and demonstrate that multiple parallel gene losses are likely responsible for the significant species tree conflict observed in the genus Echis. These results highlight the potential for gene tree parsimony analyses to be undermined by rapidly evolving multilocus gene families under strong natural selection.