A comparative study of SVDquartets and other coalescent-based species tree estimation methods

Background: Species tree estimation is challenging in the presence of incomplete lineage sorting (ILS), which can make gene trees different from the species tree. Because ILS is expected to occur and the standard concatenation approach can return incorrect trees with high support in the presence of ILS, “coalescent-based” summary methods (which first estimate gene trees and then combine gene trees into a species tree) have been developed that have theoretical guarantees of robustness to arbitrarily high amounts of ILS. Some studies have suggested that summary methods should only be used on “c-genes” (i.e., recombination-free loci) that can be extremely short (sometimes fewer than 100 sites). However, gene trees estimated on short alignments can have high estimation error, and summary methods tend to have high error on short c-genes. To address this problem, Chifman and Kubatko introduced SVDquartets, a new coalescent-based method. SVDquartets takes multi-locus unlinked single-site data, infers the quartet trees for all subsets of four species, and then combines the set of quartet trees into a species tree using a quartet amalgamation heuristic. Yet, the relative accuracy of SVDquartets to leading coalescent-based methods has not been assessed. Results: We compared SVDquartets to two leading coalescent-based methods (ASTRAL-2 and NJst), and to concatenation using maximum likelihood. We used a collection of simulated datasets, varying ILS levels, numbers of taxa, and number of sites per locus. Although SVDquartets was sometimes more accurate than ASTRAL-2 and NJst, most often the best results were obtained using ASTRAL-2, even on the shortest gene sequence alignments we explored (with only 10 sites per locus). Finally, concatenation was the most accurate of all methods under low ILS conditions. Conclusions: ASTRAL-2 generally had the best accuracy under higher ILS conditions, and concatenation had the best accuracy under the lowest ILS conditions. However, SVDquartets was competitive with the best methods under conditions with low ILS and small numbers of sites per locus. The good performance under many conditions of ASTRAL-2 in comparison to SVDquartets is surprising given the known vulnerability of ASTRAL-2 and similar methods to short gene sequences.

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The Perfect Storm: Gene Tree Estimation Error, Incomplete Lineage Sorting, and Ancient Gene Flow Explain the Most Recalcitrant Ancient Angiosperm Clade, Malpighiales

Systematic Biology ◽

10.1093/sysbio/syaa083 ◽

2020 ◽

Author(s):

Liming Cai ◽

Zhenxiang Xi ◽

Emily Moriarty Lemmon ◽

Alan R Lemmon ◽

Austin Mast ◽

...

Keyword(s):

Gene Flow ◽

Incomplete Lineage Sorting ◽

Estimation Error ◽

Gene Tree ◽

Species Tree ◽

Flowering Plant ◽

Estimation Methods ◽

Lineage Sorting ◽

Tree Estimation ◽

Perfect Storm

Abstract The genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order includes nine of the top ten most unstable nodes in angiosperms, which have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 10.0%, 34.8%, and 21.4% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.

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wQFM: Statistically Consistent Genome-scale Species Tree Estimation from Weighted Quartets

10.1101/2020.11.30.403352 ◽

2020 ◽

Author(s):

Mahim Mahbub ◽

Zahin Wahab ◽

Rezwana Reaz ◽

M. Saifur Rahman ◽

Md. Shamsuzzoha Bayzid

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Accurate Method ◽

Species Tree ◽

Estimation Methods ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Tree Estimation ◽

Source Form

AbstractMotivationSpecies tree estimation from genes sampled from throughout the whole genome is complicated due to the gene tree-species tree discordance. Incomplete lineage sorting (ILS) is one of the most frequent causes for this discordance, where alleles can coexist in populations for periods that may span several speciation events. Quartet-based summary methods for estimating species trees from a collection of gene trees are becoming popular due to their high accuracy and statistical guarantee under ILS. Generating quartets with appropriate weights, where weights correspond to the relative importance of quartets, and subsequently amalgamating the weighted quartets to infer a single coherent species tree allows for a statistically consistent way of estimating species trees. However, handling weighted quartets is challenging.ResultsWe propose wQFM, a highly accurate method for species tree estimation from multi-locus data, by extending the quartet FM (QFM) algorithm to a weighted setting. wQFM was assessed on a collection of simulated and real biological datasets, including the avian phylogenomic dataset which is one of the largest phylogenomic datasets to date. We compared wQFM with wQMC, which is the best alternate method for weighted quartet amalgamation, and with ASTRAL, which is one of the most accurate and widely used coalescent-based species tree estimation methods. Our results suggest that wQFM matches or improves upon the accuracy of wQMC and ASTRAL.AvailabilitywQFM is available in open source form at https://github.com/Mahim1997/wQFM-2020.

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The Perfect Storm: Gene Tree Estimation Error, Incomplete Lineage Sorting, and Ancient Gene Flow Explain the Most Recalcitrant Ancient Angiosperm Clade, Malpighiales

10.1101/2020.05.26.112318 ◽

2020 ◽

Author(s):

Liming Cai ◽

Zhenxiang Xi ◽

Emily Moriarty Lemmon ◽

Alan R. Lemmon ◽

Austin Mast ◽

...

Keyword(s):

Gene Flow ◽

Incomplete Lineage Sorting ◽

Estimation Error ◽

Gene Tree ◽

Species Tree ◽

Flowering Plant ◽

Estimation Methods ◽

Lineage Sorting ◽

Tree Estimation ◽

Perfect Storm

ABSTRACTThe genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order alone includes nine of the top ten most unstable nodes in angiosperms, and the recalcitrant relationships along the backbone of the order have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 15%, 52%, and 32% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.

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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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Phylogenomic terraces: presence and implication in species tree estimation from gene trees

10.1101/2020.04.19.048843 ◽

2020 ◽

Author(s):

Ishrat Tanzila Farah ◽

Md Muktadirul Islam ◽

Kazi Tasnim Zinat ◽

Atif Hasan Rahman ◽

Md Shamsuzzoha Bayzid

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Deep Coalescence ◽

Tree Estimation ◽

Tree Space ◽

Multiple Species

AbstractSpecies tree estimation from multi-locus dataset is extremely challenging, especially in the presence of gene tree heterogeneity across the genome due to incomplete lineage sorting (ILS). Summary methods have been developed which estimate gene trees and then combine the gene trees to estimate a species tree by optimizing various optimization scores. In this study, we have formalized the concept of “phylogenomic terraces” in the species tree space, where multiple species trees with distinct topologies may have exactly the same optimization score (quartet score, extra lineage score, etc.) with respect to a collection of gene trees. We investigated the presence and implication of terraces in species tree estimation from multi-locus data by taking ILS into account. We analyzed two of the most popular ILS-aware optimization criteria: maximize quartet consistency (MQC) and minimize deep coalescence (MDC). Methods based on MQC are provably statistically consistent, whereas MDC is not a consistent criterion for species tree estimation. Our experiments, on a collection of dataset simulated under ILS, indicate that MDC-based methods may achieve competitive or identical quartet consistency score as MQC but could be significantly worse than MQC in terms of tree accuracy – demonstrating the presence and affect of phylogenomic terraces. This is the first known study that formalizes the concept of phylogenomic terraces in the context of species tree estimation from multi-locus data, and reports the presence and implications of terraces in species tree estimation under ILS.

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Whole-Genome Analyses Resolve the Phylogeny of Flightless Birds (Palaeognathae) in the Presence of an Empirical Anomaly Zone

Systematic Biology ◽

10.1093/sysbio/syz019 ◽

2019 ◽

Vol 68 (6) ◽

pp. 937-955 ◽

Cited By ~ 21

Author(s):

Alison Cloutier ◽

Timothy B Sackton ◽

Phil Grayson ◽

Michele Clamp ◽

Allan J Baker ◽

...

Keyword(s):

Sequence Data ◽

Incomplete Lineage Sorting ◽

Estimation Error ◽

Gene Tree ◽

Species Tree ◽

Tree Topology ◽

Whole Genome ◽

Gene Trees ◽

Lineage Sorting ◽

Genome Analyses

Abstract Palaeognathae represent one of the two basal lineages in modern birds, and comprise the volant (flighted) tinamous and the flightless ratites. Resolving palaeognath phylogenetic relationships has historically proved difficult, and short internal branches separating major palaeognath lineages in previous molecular phylogenies suggest that extensive incomplete lineage sorting (ILS) might have accompanied a rapid ancient divergence. Here, we investigate palaeognath relationships using genome-wide data sets of three types of noncoding nuclear markers, together totaling 20,850 loci and over 41 million base pairs of aligned sequence data. We recover a fully resolved topology placing rheas as the sister to kiwi and emu + cassowary that is congruent across marker types for two species tree methods (MP-EST and ASTRAL-II). This topology is corroborated by patterns of insertions for 4274 CR1 retroelements identified from multispecies whole-genome screening, and is robustly supported by phylogenomic subsampling analyses, with MP-EST demonstrating particularly consistent performance across subsampling replicates as compared to ASTRAL. In contrast, analyses of concatenated data supermatrices recover rheas as the sister to all other nonostrich palaeognaths, an alternative that lacks retroelement support and shows inconsistent behavior under subsampling approaches. While statistically supporting the species tree topology, conflicting patterns of retroelement insertions also occur and imply high amounts of ILS across short successive internal branches, consistent with observed patterns of gene tree heterogeneity. Coalescent simulations and topology tests indicate that the majority of observed topological incongruence among gene trees is consistent with coalescent variation rather than arising from gene tree estimation error alone, and estimated branch lengths for short successive internodes in the inferred species tree fall within the theoretical range encompassing the anomaly zone. Distributions of empirical gene trees confirm that the most common gene tree topology for each marker type differs from the species tree, signifying the existence of an empirical anomaly zone in palaeognaths.

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To include or not to include: The impact of gene filtering on species tree estimation methods

10.1101/149120 ◽

2017 ◽

Cited By ~ 1

Author(s):

Erin K. Molloy ◽

Tandy Warnow

Keyword(s):

Missing Data ◽

Incomplete Lineage Sorting ◽

Estimation Error ◽

Gene Tree ◽

Species Tree ◽

Species Trees ◽

Lineage Sorting ◽

Gene Filtering ◽

Tree Estimation ◽

The Impact

AbstractSpecies tree estimation from loci sampled from multiple genomes is now common, but is challenged by the heterogeneity across the genome due to multiple processes, such as gene duplication and loss, horizontal gene transfer, and incomplete lineage sorting. Although methods for estimating species trees have been developed that address gene tree heterogeneity due to incomplete lineage sorting, many of these methods operate by combining estimated gene trees and are hence vulnerable to gene tree quality. There is also the added concern that missing data, which is frequently encountered in genome-scale datasets, will impact species tree estimation.Our study addresses the impact of gene filtering on species trees inferred from multi-gene datasets. We address these questions using a large and heterogeneous collection of simulated datasets both with and without missing data. We compare several established coalescent-based methods (ASTRAL, ASTRID, MP-EST, and SVDquartets within PAUP*) as well as unpartitioned concatenation using maximum likelihood (RAxML).Our study shows that gene tree error and missing data impact all methods (and some methods degrade more than others), but the degree of incomplete lineage sorting and gene tree estimation error impacts the absolute and relative performance of methods as well as their response to gene filtering strategies. We find that filtering genes based on the degree of missing data is either neutral or else reduces the accuracy of all five methods examined, and so is not recommended. Filtering genes based on gene tree estimation error shows somewhat different trends. Under low levels of incomplete lineage sorting, removing genes with high gene tree estimation error can improve the accuracy of summary methods, but only if not too many genes are removed. Otherwise, filtering genes tends to increase error, especially under high levels of incomplete lineage sorting. Hence, while filtering genes based on missing data is not recommended, there are conditions under which removing high error gene trees can improve species tree estimation. This study provides insights into prior studies and suggests approaches for analyzing phylogenomic datasets.

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Performance of Matrix Representation with Parsimony for Inferring Species from Gene Trees

Statistical Applications in Genetics and Molecular Biology ◽

10.2202/1544-6115.1611 ◽

2011 ◽

Vol 10 (1) ◽

Cited By ~ 6

Author(s):

Yuancheng Wang ◽

James H Degnan

Keyword(s):

Matrix Representation ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Sequence Alignments ◽

Input Gene ◽

Supertree Methods

Phylogenomic datasets often contain sequence alignments on different subsets of taxa for different genes. A major goal of phylogenetics is often to combine estimated gene trees from many loci into an overall estimate of a species tree. When data are missing for some combinations of genes and taxa, supertree methods can be used to combine gene trees on different subsets of taxa into an overall tree. However, studies of the performance of supertree methods when gene tree conflict is due to incomplete lineage sorting are needed to understand their statistical properties in this setting.We find that Matrix Representation with Parsimony (MRP), the most commonly used supertree method, can in many cases infer the species tree in spite of high levels of conflict in the input gene trees. However, for some species trees with short branches, MRP can be increasingly likely to return a tree other than the species tree as the number of loci increases. In some cases, deleting taxa at random or using estimated (rather than known) gene trees can either improve or hinder MRP for recovering the species tree.Although MRP is able to handle large amounts of conflict in the input gene trees, MRP is not statistically consistent for estimating species trees when gene trees arise under the multispecies coalescent model. However, triplet MRP is statistically consistent in this setting.

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STELAR: A statistically consistent coalescent-based species tree estimation method by maximizing triplet consistency

10.1101/594911 ◽

2019 ◽

Author(s):

Mazharul Islam ◽

Kowshika Sarker ◽

Trisha Das ◽

Rezwana Reaz ◽

Md. Shamsuzzoha Bayzid

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Estimation Method ◽

Species Tree ◽

Mcmc Methods ◽

Consistent Estimate ◽

Gene Trees ◽

Species Trees ◽

Lineage Sorting ◽

Tree Estimation

AbstractBackgroundSpecies tree estimation is frequently based on phylogenomic approaches that use multiple genes from throughout the genome. However, estimating a species tree from a collection of gene trees can be complicated due to the presence of gene tree incongruence resulting from incomplete lineage sorting (ILS), which is modelled by the multi-species coalescent process. Maximum likelihood and Bayesian MCMC methods can potentially result in accurate trees, but they do not scale well to large datasets.ResultsWe present STELAR (Species Tree Estimation by maximizing tripLet AgReement), a new fast and highly accurate statistically consistent coalescent-based method for estimating species trees from a collection of gene trees. We formalized the constrained triplet consensus (CTC) problem and showed that the solution to the CTC problem is a statistically consistent estimate of the species tree under the multi-species coalescent (MSC) model. STELAR is an efficient dynamic programming based solution to the CTC problem which is highly accurate and scalable. We evaluated the accuracy of STELAR in comparison with SuperTriplets, which is an alternate fast and highly accurate triplet-based supertree method, and with MP-EST and ASTRAL – two of the most popular and accurate coalescent-based methods. Experimental results suggest that STELAR matches the accuracy of ASTRAL and improves on MP-EST and SuperTriplets.ConclusionsTheoretical and empirical results (on both simulated and real biological datasets) suggest that STELAR is a valuable technique for species tree estimation from gene tree distributions.

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Phylogenomic species tree estimation in the presence of incomplete lineage sorting and horizontal gene transfer

10.1101/023168 ◽

2015 ◽

Cited By ~ 1

Author(s):

Ruth Davidson ◽

Pranjal Vachaspati ◽

Siavash Mirarab ◽

Tandy Warnow

Keyword(s):

Maximum Likelihood ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Estimation Methods ◽

Species Trees ◽

Lineage Sorting ◽

Tree Estimation

Background: Species tree estimation is challenged by gene tree heterogeneity resulting from biological processes such as duplication and loss, hybridization, incomplete lineage sorting (ILS), and horizontal gene transfer (HGT). Mathematical theory about reconstructing species trees in the presence of HGT alone or ILS alone suggests that quartet-based species tree methods (known to be statistically consistent under ILS, or under bounded amounts of HGT) might be effective techniques for estimating species trees when both HGT and ILS are present. Results: We evaluated several publicly available coalescent-based methods and concatenation under maximum likelihood on simulated datasets with moderate ILS and varying levels of HGT. Our study shows that two quartet-based species tree estimation methods (ASTRAL-2 and weighted Quartets MaxCut) are both highly accurate, even on datasets with high rates of HGT. In contrast, although NJst and concatenation using maximum likelihood are highly accurate under low HGT, they are less robust to high HGT rates. Conclusion: Our study shows that quartet-based species-tree estimation methods can be highly accurate under the presence of both HGT and ILS. The study suggests the possibility that some quartet-based methods might be statistically consistent under phylogenomic models of gene tree heterogeneity with both HGT and ILS. Keywords: phylogenomics; HGT; ILS; summary methods; concatenation

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