When species trees disagree: an approach consistent with the coalescent that quantifies phylogenomic support for contentious relationships

AbstractPhylogenies inferred using both concatenation- and coalescent-based analyses typically render highly congruent trees. However, when they disagree, they often differ with respect to historically contentious and evolutionarily important relationships. These relationships may also involve etiolated lineages where increased sampling is not possible. Recently, methods aimed at interrogating single relationships or trees have emerged as promising investigative tools to examine these cases. Although recent methods such as “Edge-based Phylogenomic Support analYsis” (EPSY) led to insights into both systematic error and real biological signal, whether they are consistent with the coalescent in cases with high Incomplete Lineage Sorting (ILS) has yet to be characterized. Here, we use simulations and an empirical dataset to test the performance of EPSY, concatenation, and coalescent-based summary analyses under high levels of ILS. We focused on high-ILS scenarios because these represent the typical difficult cases that researchers often face due to the prevalence of ILS in phylogenomic datasets. ILS is known to be a major cause of phylogenomic conflict, which confounds many biological conclusions that depend on a resolved phylogeny, such as inferring ancestral character states, biogeographic reconstructions, and domestication histories. Our study found that EPSY was consistent with the coalescent in a high-ILS empirical dataset. In high-ILS simulations EPSY infers the correct edge more than half the time, whereas coalescent based methods and concatenation methods inferred the actual tree 37.8% and 25% of the time, respectively. All methods have conditions under which they generate the most accurate inferences. Given the levels of ILS in simulations, 26.2% of the time no method recovered the true tree. This zone where no current method can infer the true topology is likely due to properties of the species tree, such as the length of internal edges adjacent to a conflict and/or the length of the shortest branch. Nevertheless, the EPSY approach proves to be a valuable complement to phylogenomic analyses for interrogating regions of the tree with conflicting hypotheses generated from past studies or alternative inference methods. Our analyses highlight that robust phylogenetic trees may not be possible under some scenarios regardless of method and data source.

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Disentangling Sources of Gene Tree Discordance in Phylogenomic Datasets: Testing Ancient Hybridizations in Amaranthaceae s.l

10.1101/794370 ◽

2019 ◽

Cited By ~ 2

Author(s):

Diego F. Morales-Briones ◽

Gudrun Kadereit ◽

Delphine T. Tefarikis ◽

Michael J. Moore ◽

Stephen A. Smith ◽

...

Keyword(s):

Network Inference ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Phylogenetic Network ◽

Molecular Data ◽

Species Trees ◽

Lineage Sorting ◽

Multiple Sources ◽

Gene Tree Discordance ◽

Phylogenomic Analyses

AbstractGene tree discordance in large genomic datasets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. that was previously supported by morphological, ecological, and Sanger-based molecular data. The dataset included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations.

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ASTRID: Accurate Species TRees from Internode Distances

10.1101/023036 ◽

2015 ◽

Cited By ~ 1

Author(s):

Pranjal Vachaspati ◽

Tandy Warnow

Keyword(s):

Good Accuracy ◽

Incomplete Lineage Sorting ◽

Current Method ◽

Species Tree ◽

Estimation Methods ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Tree Estimation ◽

Source Form

Background: Incomplete lineage sorting (ILS), modelled by the multi-species coalescent (MSC), is known to create discordance between gene trees and species trees, and lead to inaccurate species tree estimations unless appropriate methods are used to estimate the species tree. While many statistically consistent methods have been developed to estimate the species tree in the presence of ILS, only ASTRAL-2 and NJst have been shown to have good accuracy on large datasets. Yet, NJst is generally slower and less accurate than ASTRAL-2, and cannot run on some datasets. Results: We have redesigned NJst to enable it to run on all datasets, and we have expanded its design space so that it can be used with different distance-based tree estimation methods. The resultant method, ASTRID, is statistically consistent under the MSC model, and has accuracy that is competitive with ASTRAL-2. Furthermore, ASTRID is much faster than ASTRAL-2, completing in minutes on some datasets for which ASTRAL-2 used hours. Conclusions: ASTRID is a new coalescent-based method for species tree estimation that is competitive with the best current method in terms of accuracy, while being much faster. ASTRID is available in open source form on github.

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PoMo: An Allele Frequency-based Approach for Species Tree Estimation

10.1101/016360 ◽

2015 ◽

Author(s):

Nicola De Maio ◽

Dominik Schrempf ◽

Carolin Kosiol

Keyword(s):

Allele Frequency ◽

Phylogenetic Trees ◽

Incomplete Lineage Sorting ◽

Species Tree ◽

Efficient Estimation ◽

Species Variation ◽

Species Trees ◽

Lineage Sorting ◽

Genome Wide ◽

Tree Estimation

Incomplete lineage sorting can cause incongruencies of the overall species-level phylogenetic tree with the phylogenetic trees for individual genes or genomic segments. If these incongruencies are not accounted for, it is possible to incur several biases in species tree estimation. Here, we present a simple maximum likelihood approach that accounts for ancestral variation and incomplete lineage sorting. We use a POlymorphisms-aware phylogenetic MOdel (PoMo) that we have recently shown to efficiently estimate mutation rates and fixation biases from within and between-species variation data. We extend this model to perform efficient estimation of species trees. We test the performance of PoMo in several different scenarios of incomplete lineage sorting using simulations and compare it with existing methods both in accuracy and computational speed. In contrast to other approaches, our model does not use coalescent theory but is allele-frequency based. We show that PoMo is well suited for genome-wide species tree estimation and that on such data it is more accurate than previous approaches.

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Phylogenomic data reveal hard polytomies across the backbone of the large genus Solanum (Solanaceae)

10.1101/2021.03.25.436973 ◽

2021 ◽

Author(s):

Edeline Gagnon ◽

Rebecca Hilgenhof ◽

Andr&eacutes Orejuela ◽

Angela McDonnell ◽

Gaurav Sablok ◽

...

Keyword(s):

Phylogenetic Trees ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Flowering Plant ◽

Gene Trees ◽

Species Trees ◽

Nuclear Target ◽

Lineage Sorting ◽

Target Capture ◽

Gene Tree Discordance

Increased volumes of phylogenomic data have revealed incongruent topologies in gene trees, both between and within genomes across many organisms. Some of these incongruences indicate polytomies that may remain impossible to resolve. Here, widespread gene-tree discordance is uncovered along the backbone of Solanum, one of the largest flowering plant genera that includes the cultivated potato, tomato, and eggplant, as well as 24 minor crop plants. First, a densely sampled species-level phylogeny of Solanum is built using unpublished and publicly available Sanger sequences comprising 60% of all accepted species (742 spp.) and nine regions (ITS, waxy, and seven plastid markers). The robustness of the Sanger-based topology is tested by examining a plastome dataset with 140 species and a nuclear target-capture dataset with 39 species of Solanum. Clear incongruences between species trees generated from the supermatrix, plastome, and nuclear target-capture datasets are revealed. Discordance within the plastome and target-capture dataset are found at different evolutionary depths in three different areas along the backbone of these phylogenetic trees, with polytomy tests suggesting that most of these nodes have short branches and should be collapsed. We argue that incomplete lineage sorting due to rapid diversification is the most likely cause behind these polytomies, and that embracing the uncertainty that underlies them is crucial to depict the evolution of large and rapidly radiating lineages.

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Analyzing contentious relationships and outlier genes in phylogenomics

10.1101/115774 ◽

2017 ◽

Cited By ~ 3

Author(s):

Joseph F. Walker ◽

Joseph W. Brown ◽

Stephen A. Smith

Keyword(s):

Incomplete Lineage Sorting ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Tree Inference ◽

Small Set ◽

Tree Methods ◽

Edge Based ◽

Species Tree Inference

ABSTRACTRecent studies have demonstrated that conflict is common among gene trees in phylogenomic studies, and that less than one percent of genes may ultimately drive species tree inference in supermatrix analyses. Here, we examined two datasets where supermatrix and coalescent-based species trees conflict. We identified two highly influential “outlier” genes in each dataset. When removed from each dataset, the inferred supermatrix trees matched the topologies obtained from coalescent analyses. We also demonstrate that, while the outlier genes in the vertebrate dataset have been shown in a previous study to be the result of errors in orthology detection, the outlier genes from a plant dataset did not exhibit any obvious systematic error and therefore may be the result of some biological process yet to be determined. While topological comparisons among a small set of alternate topologies can be helpful in discovering outlier genes, they can be limited in several ways, such as assuming all genes share the same topology. Coalescent species tree methods relax this assumption but do not explicitly facilitate the examination of specific edges. Coalescent methods often also assume that conflict is the result of incomplete lineage sorting (ILS). Here we explored a framework that allows for quickly examining alternative edges and support for large phylogenomic datasets that does not assume a single topology for all genes. For both datasets, these analyses provided detailed results confirming the support for coalescent-based topologies. This framework suggests that we can improve our understanding of the underlying signal in phylogenomic datasets by asking more targeted edge-based questions.

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Impact of Ghost Introgression on Coalescent-based Species Tree Inference and Estimation of Divergence Time

10.1101/2022.01.11.475787 ◽

2022 ◽

Author(s):

XiaoXu Pang ◽

Da-Yong Zhang

Keyword(s):

Incomplete Lineage Sorting ◽

Divergence Time ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Multispecies Coalescent ◽

Tree Inference ◽

Tree Methods ◽

The Impact

The species studied in any evolutionary investigation generally constitute a very small proportion of all the species currently existing or that have gone extinct. It is therefore likely that introgression, which is widespread across the tree of life, involves "ghosts," i.e., unsampled, unknown, or extinct lineages. However, the impact of ghost introgression on estimations of species trees has been rarely studied and is thus poorly understood. In this study, we use mathematical analysis and simulations to examine the robustness of species tree methods based on a multispecies coalescent model under gene flow sourcing from an extant or ghost lineage. We found that very low levels of extant or ghost introgression can result in anomalous gene trees (AGTs) on three-taxon rooted trees if accompanied by strong incomplete lineage sorting (ILS). In contrast, even massive introgression, with more than half of the recipient genome descending from the donor lineage, may not necessarily lead to AGTs. In cases involving an ingroup lineage (defined as one that diverged no earlier than the most basal species under investigation) acting as the donor of introgression, the time of root divergence among the investigated species was either underestimated or remained unaffected, but for the cases of outgroup ghost lineages acting as donors, the divergence time was generally overestimated. Under many conditions of ingroup introgression, the stronger the ILS was, the higher was the accuracy of estimating the time of root divergence, although the topology of the species tree is more prone to be biased by the effect of introgression.

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How to Tackle Phylogenetic Discordance in Recent and Rapidly Radiating Groups? Developing a Workflow Using Loricaria (Asteraceae) as an Example

Frontiers in Plant Science ◽

10.3389/fpls.2021.765719 ◽

2022 ◽

Vol 12 ◽

Author(s):

Martha Kandziora ◽

Petr Sklenář ◽

Filip Kolář ◽

Roswitha Schmickl

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Secondary Contact ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Phylogenetic Discordance ◽

Gene Tree Discordance ◽

High Degree

A major challenge in phylogenetics and -genomics is to resolve young rapidly radiating groups. The fast succession of species increases the probability of incomplete lineage sorting (ILS), and different topologies of the gene trees are expected, leading to gene tree discordance, i.e., not all gene trees represent the species tree. Phylogenetic discordance is common in phylogenomic datasets, and apart from ILS, additional sources include hybridization, whole-genome duplication, and methodological artifacts. Despite a high degree of gene tree discordance, species trees are often well supported and the sources of discordance are not further addressed in phylogenomic studies, which can eventually lead to incorrect phylogenetic hypotheses, especially in rapidly radiating groups. We chose the high-Andean Asteraceae genus Loricaria to shed light on the potential sources of phylogenetic discordance and generated a phylogenetic hypothesis. By accounting for paralogy during gene tree inference, we generated a species tree based on hundreds of nuclear loci, using Hyb-Seq, and a plastome phylogeny obtained from off-target reads during target enrichment. We observed a high degree of gene tree discordance, which we found implausible at first sight, because the genus did not show evidence of hybridization in previous studies. We used various phylogenomic analyses (trees and networks) as well as the D-statistics to test for ILS and hybridization, which we developed into a workflow on how to tackle phylogenetic discordance in recent radiations. We found strong evidence for ILS and hybridization within the genus Loricaria. Low genetic differentiation was evident between species located in different Andean cordilleras, which could be indicative of substantial introgression between populations, promoted during Pleistocene glaciations, when alpine habitats shifted creating opportunities for secondary contact and hybridization.

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MSCquartets 1.0: Quartet methods for species trees and networks under the multispecies coalescent model in R

Bioinformatics ◽

10.1093/bioinformatics/btaa868 ◽

2020 ◽

Author(s):

John A Rhodes ◽

Hector Baños ◽

Jonathan D Mitchell ◽

Elizabeth S Allman

Keyword(s):

Network Inference ◽

Incomplete Lineage Sorting ◽

R Package ◽

Species Tree ◽

Supplementary Information ◽

Species Trees ◽

Lineage Sorting ◽

Coalescent Model ◽

Multispecies Coalescent ◽

Tree Inference

Abstract Summary MSCquartets is an R package for species tree hypothesis testing, inference of species trees, and inference of species networks under the Multispecies Coalescent model of incomplete lineage sorting and its network analog. Input for these analyses are collections of metric or topological locus trees which are then summarized by the quartets displayed on them. Results of hypothesis tests at user-supplied levels are displayed in a simplex plot by color-coded points. The package implements the QDC and WQDC algorithms for topological and metric species tree inference, and the NANUQ algorithm for level-1 topological species network inference, all of which give statistically consistent estimators under the model. Availability MSCquartets is available through the Comprehensive R Archive Network: https://CRAN.R-project.org/package=MSCquartets. Supplementary information Supplementary materials, including example data and analyses, are incorporated into the package.

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Disentangling Sources of Gene Tree Discordance in Phylogenomic Data Sets: Testing Ancient Hybridizations in Amaranthaceae s.l

Systematic Biology ◽

10.1093/sysbio/syaa066 ◽

2020 ◽

Cited By ~ 1

Author(s):

Diego F Morales-Briones ◽

Gudrun Kadereit ◽

Delphine T Tefarikis ◽

Michael J Moore ◽

Stephen A Smith ◽

...

Keyword(s):

Network Inference ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Phylogenetic Network ◽

Species Tree ◽

Data Sets ◽

Species Trees ◽

Lineage Sorting ◽

Data Set ◽

Gene Tree Discordance

Abstract Gene tree discordance in large genomic data sets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. that was previously supported by morphological, ecological, and Sanger-based molecular data. The data set included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations. [Amaranthaceae; gene tree discordance; hybridization; incomplete lineage sorting; phylogenomics; species network; species tree; transcriptomics.]

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Species Tree Inference under the Multispecies Coalescent on Data with Paralogs is Accurate

10.1101/498378 ◽

2018 ◽

Cited By ~ 10

Author(s):

Zhi Yan ◽

Peng Du ◽

Matthew W. Hahn ◽

Luay Nakhleh

Keyword(s):

Incomplete Lineage Sorting ◽

Single Copy ◽

Species Tree ◽

Biological Data ◽

Lineage Sorting ◽

Multispecies Coalescent ◽

Gene Copies ◽

Tree Inference ◽

Inference Methods ◽

Species Tree Inference

AbstractThe multispecies coalescent (MSC) has emerged as a powerful and desirable framework for species tree inference in phylogenomic studies. Under this framework, the data for each locus is assumed to consist of orthologous, single-copy genes, and heterogeneity across loci is assumed to be due to incomplete lineage sorting (ILS). These assumptions have led biologists that use ILS-aware inference methods, whether based directly on the MSC or proven to be statistically consistent under it (collectively referred to here as MSC-based methods), to exclude all loci that are present in more than a single copy in any of the studied genomes. Furthermore, such analyses entail orthology assignment to avoid the potential of hidden paralogy in the data. The question we seek to answer in this study is: What happens if one runs such species tree inference methods on data where paralogy is present, in addition to or without ILS being present? Through simulation studies and analyses of two biological data sets, we show that running such methods on data with paralogs provide very accurate results, either by treating all gene copies within a family as alleles from multiple individuals or by randomly selecting one copy per species. Our results have significant implications for the use of MSC-based phylogenomic analyses, demonstrating that they do not have to be restricted to single-copy loci, thus greatly increasing the amount of data that can be used. [Multispecies coalescent; incomplete lineage sorting; gene duplication and loss; orthology; paralogy.]

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