The Impact of Cross-Species Gene Flow on Species Tree Estimation

Abstract Recent analyses of genomic sequence data suggest cross-species gene flow is common in both plants and animals, posing challenges to species tree estimation. We examine the levels of gene flow needed to mislead species tree estimation with three species and either episodic introgressive hybridization or continuous migration between an outgroup and one ingroup species. Several species tree estimation methods are examined, including the majority-vote method based on the most common gene tree topology (with either the true or reconstructed gene trees used), the UPGMA method based on the average sequence distances (or average coalescent times) between species, and the full-likelihood method based on multilocus sequence data. Our results suggest that the majority-vote method based on gene tree topologies is more robust to gene flow than the UPGMA method based on coalescent times and both are more robust than likelihood assuming a multispecies coalescent (MSC) model with no cross-species gene flow. Comparison of the continuous migration model with the episodic introgression model suggests that a small amount of gene flow per generation can cause drastic changes to the genetic history of the species and mislead species tree methods, especially if the species diverged through radiative speciation events. Estimates of parameters under the MSC with gene flow suggest that African mosquito species in the Anopheles gambiae species complex constitute such an example of extreme impact of gene flow on species phylogeny. [IM; introgression; migration; MSci; multispecies coalescent; species tree.]

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The Impact of Cross-Species Gene Flow on Species Tree Estimation

10.1101/820019 ◽

2019 ◽

Cited By ~ 1

Author(s):

Xiyun Jiao ◽

Thomas Flouris ◽

Bruce Rannala ◽

Ziheng Yang

Keyword(s):

Gene Flow ◽

Sequence Data ◽

Majority Vote ◽

Gene Tree ◽

Species Tree ◽

Likelihood Method ◽

Estimation Methods ◽

Vote Method ◽

Tree Estimation ◽

The Impact

ABSTRACTRecent analyses of genomic sequence data suggest cross-species gene flow is common in both plants and animals, posing challenges to species tree inference. We examine the levels of gene flow needed to mislead species tree estimation with three species and either episodic introgressive hybridization or continuous migration between an outgroup and one ingroup species. Several species tree estimation methods are examined, including the majority-vote method based on the most common gene tree topology (with either the true or reconstructed gene trees used), the UPGMA method based on the average sequence distances (or average coalescent times) between species, and the full-likelihood method based on multi-locus sequence data. Our results suggest that the majority-vote method is more robust to gene flow than the UPGMA method and both are more robust than likelihood assuming a multispecies coalescent (MSC) model with no cross-species gene flow. A small amount of introgression or migration can mislead species tree methods if the species diverged through speciation events separated by short time intervals. Estimates of parameters under the MSC with gene flow suggest the Anopheles gambia African mosquito species complex is an example where gene flow greatly impacts species phylogeny.

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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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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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The BPP program for species tree estimation and species delimitation

Current Zoology ◽

10.1093/czoolo/61.5.854 ◽

2015 ◽

Vol 61 (5) ◽

pp. 854-865 ◽

Cited By ~ 314

Author(s):

Ziheng Yang

Keyword(s):

Species Delimitation ◽

Genomic Sequence ◽

Sequence Data ◽

Species Tree ◽

Joint Analysis ◽

Coalescent Model ◽

Species Phylogeny ◽

Multispecies Coalescent ◽

Tree Estimation ◽

Nuclear Loci

Abstract This paper provides an overview and a tutorial of the BPP program, which is a Bayesian MCMC program for analyzing multi-locus genomic sequence data under the multispecies coalescent model. An example dataset of five nuclear loci from the East Asian brown frogs is used to illustrate four different analyses, including estimation of species divergence times and population size parameters under the multispecies coalescent model on a fixed species phylogeny (A00), species tree estimation when the assignment and species delimitation are fixed (A01), species delimitation using a fixed guide tree (A10), and joint species delimitation and species-tree estimation or unguided species delimitation (A11). For the joint analysis (A11), two new priors are introduced, which assign uniform probabilities for the different numbers of delimited species, which may be useful when assignment, species delimitation, and species phylogeny are all inferred in one joint analysis. The paper ends with a discussion of the assumptions, the strengths and weaknesses of the BPP analysis.

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Complexity of the simplest species tree problem

Molecular Biology and Evolution ◽

10.1093/molbev/msab009 ◽

2021 ◽

Author(s):

Tianqi Zhu ◽

Ziheng Yang

Keyword(s):

Maximum Likelihood ◽

Estimation Error ◽

Gene Tree ◽

Species Tree ◽

Ancestral Population ◽

Statistical Efficiency ◽

Multispecies Coalescent ◽

Full Likelihood ◽

Tree Methods ◽

Tree Estimation

Abstract The multispecies coalescent (MSC) model provides a natural framework for species tree estimation accounting for gene-tree conflicts. While a number of species tree methods under the MSC have been suggested and evaluated using simulation, their statistical properties remain poorly understood. Here we use mathematical analysis aided by computer simulation to examine the identifiability, consistency, and efficiency of different species tree methods in the case of three species and three sequences under the molecular clock. We consider four major species-tree methods including concatenation, two-step, independent-sites maximum likelihood (ISML) and maximum likelihood (ML). We develop approximations that predict that the probit transform of the species tree estimation error decreases linearly with the square root of the number of loci. Even in this simplest case major differences exist among the methods. Fulllikelihood methods are considerably more efficient than summary methods such as concatenation and two-step. They also provide estimates of important parameters such as species divergence times and ancestral population sizes while these parameters are not identifiable by summary methods. Our results highlight the need to improve the statistical efficiency of summary methods and the computational efficiency of full likelihood methods of species tree estimation.

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PRANC: ML species tree estimation from the ranked gene trees under coalescence

Bioinformatics ◽

10.1093/bioinformatics/btaa605 ◽

2020 ◽

Vol 36 (18) ◽

pp. 4819-4821

Author(s):

Anastasiia Kim ◽

James H Degnan

Keyword(s):

Maximum Likelihood ◽

Gene Tree ◽

Species Tree ◽

Supplementary Information ◽

Supplementary Data ◽

Gene Trees ◽

Multispecies Coalescent ◽

Branch Lengths ◽

Tree Topologies ◽

Tree Estimation

Abstract Summary PRANC computes the Probabilities of RANked gene tree topologies under the multispecies coalescent. A ranked gene tree is a gene tree accounting for the temporal ordering of internal nodes. PRANC can also estimate the maximum likelihood (ML) species tree from a sample of ranked or unranked gene tree topologies. It estimates the ML tree with estimated branch lengths in coalescent units. Availability and implementation PRANC is written in C++ and freely available at github.com/anastasiiakim/PRANC. Supplementary information Supplementary data are available at Bioinformatics online.

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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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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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Why concatenation fails in the anomaly zone

10.1101/116509 ◽

2017 ◽

Cited By ~ 2

Author(s):

Fábio K. Mendes ◽

Matthew W. Hahn

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Species Tree ◽

Estimation Methods ◽

Species Trees ◽

Lineage Sorting ◽

Common Gene ◽

Tree Estimation ◽

Genome Scale ◽

Future Work

AbstrctGenome-scale sequencing has been of great benefit in recovering species trees, but has not provided final answers. Despite the rapid accumulation of molecular sequences, resolving short and deep branches of the tree of life has remained a challenge, and has prompted the development of new strategies that can make the best use of available data. One such strategy – the concatenation of gene alignments – can be successful when coupled with many tree estimation methods, but has also been shown to fail when there are high levels of incomplete lineage sorting. Here, we focus on the failure of likelihood-based methods in retrieving a rooted, asymmetric four-taxon species tree from concatenated data when the species tree is in or near the anomaly zone – a region of parameter space where the most common gene tree does not match the species tree because of incomplete lineage sorting. First, we use coalescent theory to prove that most informative sites will support the species tree in the anomaly zone, and that as a consequence maximum-parsimony succeeds in recovering the species tree from concatenated data. We further show that maximum-likelihood tree estimation from concatenated data fails both inside and outside the anomaly zone, and that this failure is unconnected to the frequency of the most common gene tree. We provide support for a hypothesis that likelihood-based methods fail in and near the anomaly zone because discordant sites on the species tree have a lower likelihood than those that are discordant on alternative topologies. Our results confirm and extend previous reports of the failure and success of likelihood- and parsimony-based methods, and highlight avenues for future work improving the performance of methods aimed at recovering species tree.

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Retroposon Insertions within a Multispecies Coalescent Framework Suggest that Ratite Phylogeny is not in the ‘Anomaly Zone’

10.1101/643296 ◽

2019 ◽

Cited By ~ 3

Author(s):

Mark S. Springer ◽

John Gatesy

Keyword(s):

Phylogenetic Analysis ◽

Sequence Data ◽

Gene Tree ◽

Reconstruction Error ◽

Species Tree ◽

Neutral Evolution ◽

Gene Trees ◽

Tree Reconstruction ◽

Multispecies Coalescent ◽

Branch Lengths

ABSTRACTSummary coalescence methods were developed to address the negative impacts of incomplete lineage sorting on species tree estimation with concatenation. Coalescence methods are statistically consistent if certain requirements are met including no intralocus recombination, neutral evolution, and no gene tree reconstruction error. However, the assumption of no intralocus recombination may not hold for many DNA sequence data sets, and neutral evolution is not the rule for genetic markers that are commonly employed in phylogenomic coalescence analyses. Most importantly, the assumption of no gene tree reconstruction error is routinely violated, especially for rapid radiations that are deep in the Tree of Life. With the sequencing of complete genomes and novel pipelines, phylogenetic analysis of retroposon insertions has emerged as a valuable alternative to sequence-based phylogenetic analysis. Retroposon insertions avoid or reduce several problems that beset analysis of sequence data with summary coalescence methods: 1) intralocus recombination is avoided because retroposon insertions are singular evolutionary events, 2) neutral evolution is approximated in many cases, and 3) gene tree reconstruction errors are rare because retroposons have low rates of homoplasy. However, the analysis of retroposons within a multispecies coalescent framework has not been realized. Here, we propose a simple workaround in which a retroposon insertion matrix is first transformed into a series of incompletely resolved gene trees. Next, the program ASTRAL is used to estimate a species tree in the statistically consistent framework of the multispecies coalescent. The inferred species tree includes support scores at all nodes and internal branch lengths in coalescent units. As a test case, we analyzed a retroposon dataset for palaeognath birds (ratites and tinamous) with ASTRAL and compared the resulting species tree to an MP-EST species tree for the same clade derived from thousands of sequence-based gene trees. The MP-EST species tree suggests an empirical case of the ‘anomaly zone’ with three very short internal branches at the base of Palaeognathae, and as predicted for anomaly zone conditions, the MP-EST species tree differs from the most common gene tree. Although identical in topology to the MP-EST tree, the ASTRAL species tree based on retroposons shows branch lengths that are much longer and incompatible with anomaly zone conditions. Simulation of gene trees from the retroposon-based species tree reveals that the most common gene tree matches the species tree. We contend that the wide discrepancies in branch lengths between sequence-based and retroposon-based species trees are explained by the greater accuracy of retroposon gene trees (bipartitions) relative to sequence-based gene trees. Coalescence analysis of retroposon data provides a promising alternative to the status quo by reducing gene tree reconstruction error that can have large impacts on both branch length estimates and evolutionary interpretations.

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