A divide-and-conquer phylogenomic approach based on character supermatrices resolves early steps in the evolution of the Archaea

Abstract Background The recent rise in cultivation-independent genome sequencing has provided key material to explore uncharted branches of the Tree of Life. This has been particularly spectacular concerning the Archaea, projecting them at the center stage as prominently relevant to understand early stages in evolution and the emergence of fundamental metabolisms as well as the origin of eukaryotes. Yet, resolving deep divergences remains a challenging task due to well-known tree-reconstruction artefacts and biases in extracting robust ancient phylogenetic signal, notably when analyzing data sets including the three Domains of Life. Among the various strategies aimed at mitigating these problems, divide-and-conquer approaches remain poorly explored, and have been primarily based on reconciliation among single gene trees which however notoriously lack ancient phylogenetic signal. Results We analyzed sub-sets of full supermatrices covering the whole Tree of Life with specific taxonomic sampling to robustly resolve different parts of the archaeal phylogeny in light of their current diversity. Our results strongly support the existence and early emergence of two main clades, Cluster I and Cluster II, which we name Ouranosarchaea and Gaiarchaea, and we clarify the placement of important novel archaeal lineages within these two clades. However, the monophyly and branching of the fast evolving nanosized DPANN members remains unclear and worth of further study. Conclusions We inferred a well resolved rooted phylogeny of the Archaea that includes all recently described phyla of high taxonomic rank. This phylogeny represents a valuable reference to study the evolutionary events associated to the early steps of the diversification of the archaeal domain. Beyond the specifics of archaeal phylogeny, our results demonstrate the power of divide-and-conquer approaches to resolve deep phylogenetic relationships, which should be applied to progressively resolve the entire Tree of Life.

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A Novel Approach to Investigate the Effect of Tree Reconstruction Artifacts in Single-Gene Analysis Clarifies Opsin Evolution in Nonbilaterian Metazoans

Genome Biology and Evolution ◽

10.1093/gbe/evaa015 ◽

2020 ◽

Vol 12 (2) ◽

pp. 3906-3916 ◽

Cited By ~ 1

Author(s):

James F Fleming ◽

Roberto Feuda ◽

Nicholas W Roberts ◽

Davide Pisani

Keyword(s):

Phylogenetic Signal ◽

Single Gene ◽

G Protein Coupled Receptors ◽

Data Sets ◽

Gene Trees ◽

Tree Reconstruction ◽

Phylogenetic Information ◽

Novel Approach ◽

Gene Data ◽

G Protein Coupled

Abstract Our ability to correctly reconstruct a phylogenetic tree is strongly affected by both systematic errors and the amount of phylogenetic signal in the data. Current approaches to tackle tree reconstruction artifacts, such as the use of parameter-rich models, do not translate readily to single-gene alignments. This, coupled with the limited amount of phylogenetic information contained in single-gene alignments, makes gene trees particularly difficult to reconstruct. Opsin phylogeny illustrates this problem clearly. Opsins are G-protein coupled receptors utilized in photoreceptive processes across Metazoa and their protein sequences are roughly 300 amino acids long. A number of incongruent opsin phylogenies have been published and opsin evolution remains poorly understood. Here, we present a novel approach, the canary sequence approach, to investigate and potentially circumvent errors in single-gene phylogenies. First, we demonstrate our approach using two well-understood cases of long-branch attraction in single-gene data sets, and simulations. After that, we apply our approach to a large collection of well-characterized opsins to clarify the relationships of the three main opsin subfamilies.

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Genomic Characterization and Curation of UCEs Improves Species Tree Reconstruction

Systematic Biology ◽

10.1093/sysbio/syaa063 ◽

2020 ◽

Author(s):

Matthew H Van Dam ◽

James B Henderson ◽

Lauren Esposito ◽

Michelle Trautwein

Keyword(s):

Marine Invertebrates ◽

Phylogenetic Analyses ◽

Single Gene ◽

Gene Tree ◽

Single Copy ◽

Species Tree ◽

Bootstrap Support ◽

Gene Trees ◽

Species Trees ◽

Tree Reconstruction

Abstract Ultraconserved genomic elements (UCEs) are generally treated as independent loci in phylogenetic analyses. The identification pipeline for UCE probes does not require prior knowledge of genetic identity, only selecting loci that are highly conserved, single copy, without repeats, and of a particular length. Here, we characterized UCEs from 11 phylogenomic studies across the animal tree of life, from birds to marine invertebrates. We found that within vertebrate lineages, UCEs are mostly intronic and intergenic, while in invertebrates, the majority are in exons. We then curated four different sets of UCE markers by genomic category from five different studies including: birds, mammals, fish, Hymenoptera (ants, wasps, and bees), and Coleoptera (beetles). Of genes captured by UCEs, we find that many are represented by two or more UCEs, corresponding to nonoverlapping segments of a single gene. We considered these UCEs to be nonindependent, merged all UCEs that belonged to a particular gene, constructed gene and species trees, and then evaluated the subsequent effect of merging cogenic UCEs on gene and species tree reconstruction. Average bootstrap support for merged UCE gene trees was significantly improved across all data sets apparently driven by the increase in loci length. Additionally, we conducted simulations and found that gene trees generated from merged UCEs were more accurate than those generated by unmerged UCEs. As loci length improves gene tree accuracy, this modest degree of UCE characterization and curation impacts downstream analyses and demonstrates the advantages of incorporating basic genomic characterizations into phylogenomic analyses. [Anchored hybrid enrichment; ants; ASTRAL; bait capture; carangimorph; Coleoptera; conserved nonexonic elements; exon capture; gene tree; Hymenoptera; mammal; phylogenomic markers; songbird; species tree; ultraconserved elements; weevils.]

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Genomic characterization and curation of UCEs improves species tree reconstruction

10.1101/828335 ◽

2019 ◽

Author(s):

Matthew H. Van Dam ◽

James B. Henderson ◽

Lauren Esposito ◽

Michelle Trautwein

Keyword(s):

Marine Invertebrates ◽

Phylogenetic Analyses ◽

Single Gene ◽

Single Copy ◽

Species Tree ◽

Bootstrap Support ◽

Gene Trees ◽

Species Trees ◽

Tree Reconstruction ◽

Phylogenomic Analyses

ABSTRACTUltraconserved genomic elements (UCEs), are generally treated as independent loci in phylogenetic analyses. The identification pipeline for UCE probes is agnostic to genetic identity, only selecting loci that are highly conserved, single copy, without repeats, and of a particular length. Here we characterized UCEs from 12 phylogenomic studies across the animal tree of life, from birds to marine invertebrates. We found that within vertebrate lineages, UCEs are mostly intronic and intergenic, while in invertebrates, the majority are in exons. We then curated 4 different sets of UCE markers by genomic category from 5 different studies including; birds, mammals, fish, Hymenoptera (ants, wasps and bees) and Coleoptera (beetles). Of genes captured by UCEs, we find that many are represented by 2 or more UCEs, corresponding to non-overlapping segments of a single gene. We considered these UCEs to be non-independent, merged all UCEs that belonged to a particular gene, constructed gene and species trees, and then evaluated the subsequent effect of merging co-genic UCEs on gene and species tree reconstruction. Average bootstrap support for merged UCE gene trees were significantly improved across all datasets. Increased loci length appears to drive this increase in bootstrap support. Additionally, we found that gene trees generated from merged UCEs were more accurate than those generated by unmerged and randomly merged UCEs, based on our simulation study. This modest degree of UCE characterization and curation impacts downstream analyses and demonstrates the advantages of incorporating basic genomic characterizations into phylogenomic analyses.

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Evaluating fast maximum likelihood-based phylogenetic programs using empirical phylogenomic data sets

10.1101/142323 ◽

2017 ◽

Cited By ~ 3

Author(s):

Xiaofan Zhou ◽

Xingxing Shen ◽

Chris Todd Hittinger ◽

Antonis Rokas

Keyword(s):

Maximum Likelihood ◽

Phylogenetic Signal ◽

Single Gene ◽

Gene Tree ◽

Species Tree ◽

Data Matrix ◽

Systematic Evaluation ◽

Data Sets ◽

Tree Inference ◽

Data Matrices

AbstractPhylogenetics has witnessed dramatic increases in the sizes of data matrices assembled to resolve branches of the tree of life, motivating the development of programs for fast, yet accurate, inference. For example, several different fast programs have been developed in the very popular maximum likelihood framework, including RAxML/ExaML, PhyML, IQ-TREE, and FastTree. Although these four programs are widely used, a systematic evaluation and comparison of their performance using empirical genome-scale data matrices has so far been lacking. To address this question, we evaluated these four programs on 19 empirical phylogenomic data sets from diverse animal, plant, and fungal lineages with respect to likelihood maximization, tree topology, and computational speed. For single-gene tree inference, we found that the more exhaustive and slower strategies (ten searches per alignment) outperformed faster strategies (one tree search per alignment) using RAxML, PhyML, or IQ-TREE. Interestingly, single-gene trees inferred by the three programs yielded comparable coalescent-based species tree estimations. For concatenation–based species tree inference, IQ-TREE consistently achieved the best-observed likelihoods for all data sets, and RAxML/ExaML was a close second. In contrast, PhyML often failed to complete concatenation-based analyses, whereas FastTree was the fastest but generated lower likelihood values and more dissimilar tree topologies in both types of analyses. Finally, data matrix properties, such as the number of taxa and the strength of phylogenetic signal, sometimes substantially influenced the relative performance of the programs. Our results provide real-world gene and species tree phylogenetic inference benchmarks to inform the design and execution of large-scale phylogenomic data analyses.

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Archaea and the prokaryote-to-eukaryote transition

Microbiology and Molecular Biology Reviews ◽

10.1128/mmbr.61.4.456-502.1997 ◽

1997 ◽

Vol 61 (4) ◽

pp. 456-502

Author(s):

J R Brown ◽

W F Doolittle

Keyword(s):

Gene Evolution ◽

Phylogenetic Analyses ◽

General Pattern ◽

Tree Of Life ◽

Gene Trees ◽

Universal Tree ◽

The Status ◽

Molecular Phylogenetic ◽

Domains Of Life ◽

Cumulative Knowledge

Since the late 1970s, determining the phylogenetic relationships among the contemporary domains of life, the Archaea (archaebacteria), Bacteria (eubacteria), and Eucarya (eukaryotes), has been central to the study of early cellular evolution. The two salient issues surrounding the universal tree of life are whether all three domains are monophyletic (i.e., all equivalent in taxanomic rank) and where the root of the universal tree lies. Evaluation of the status of the Archaea has become key to answering these questions. This review considers our cumulative knowledge about the Archaea in relationship to the Bacteria and Eucarya. Particular attention is paid to the recent use of molecular phylogenetic approaches to reconstructing the tree of life. In this regard, the phylogenetic analyses of more than 60 proteins are reviewed and presented in the context of their participation in major biochemical pathways. Although many gene trees are incongruent, the majority do suggest a sisterhood between Archaea and Eucarya. Altering this general pattern of gene evolution are two kinds of potential interdomain gene transferrals. One horizontal gene exchange might have involved the gram-positive Bacteria and the Archaea, while the other might have occurred between proteobacteria and eukaryotes and might have been mediated by endosymbiosis.

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Archaea: The First Domain of Diversified Life

Archaea ◽

10.1155/2014/590214 ◽

2014 ◽

Vol 2014 ◽

pp. 1-26 ◽

Cited By ~ 12

Author(s):

Gustavo Caetano-Anollés ◽

Arshan Nasir ◽

Kaiyue Zhou ◽

Derek Caetano-Anollés ◽

Jay E. Mittenthal ◽

...

Keyword(s):

Phylogenetic Signal ◽

Tree Of Life ◽

Early History ◽

Process Models ◽

Evolutionary Models ◽

Tree Reconstruction ◽

Evolutionary Studies ◽

History Of ◽

Phylogenetic Framework ◽

Conceptual Difficulties

The study of the origin of diversified life has been plagued by technical and conceptual difficulties, controversy, and apriorism. It is now popularly accepted that the universal tree of life is rooted in the akaryotes and that Archaea and Eukarya are sister groups to each other. However, evolutionary studies have overwhelmingly focused on nucleic acid and protein sequences, which partially fulfill only two of the three main steps of phylogenetic analysis, formulation of realistic evolutionary models, and optimization of tree reconstruction. In the absence of character polarization, that is, the ability to identify ancestral and derived character states, any statement about the rooting of the tree of life should be considered suspect. Here we show that macromolecular structure and a new phylogenetic framework of analysis that focuses on the parts of biological systems instead of the whole provide both deep and reliable phylogenetic signal and enable us to put forth hypotheses of origin. We review over a decade of phylogenomic studies, which mine information in a genomic census of millions of encoded proteins and RNAs. We show how the use of process models of molecular accumulation that comply with Weston’s generality criterion supports a consistent phylogenomic scenario in which the origin of diversified life can be traced back to the early history of Archaea.

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Quartet-based computations of internode certainty provide accurate and robust measures of phylogenetic incongruence

10.1101/168526 ◽

2017 ◽

Cited By ~ 8

Author(s):

Xiaofan Zhou ◽

Sarah Lutteropp ◽

Lucas Czech ◽

Alexandros Stamatakis ◽

Moritz von Looz ◽

...

Keyword(s):

Phylogenetic Relationships ◽

Phylogenetic Trees ◽

Phylogenetic Signal ◽

Simulated Data ◽

Data Sets ◽

Gene Trees ◽

Branch Support ◽

Robust Measures ◽

Genome Scale ◽

Scale Data

AbstractIncongruence, or topological conflict, is prevalent in genome-scale data sets but relatively few measures have been developed to quantify it. Internode Certainty (IC) and related measures were recently introduced to explicitly quantify the level of incongruence of a given internode (or internal branch) among a set of phylogenetic trees and complement regular branch support statistics in assessing the confidence of the inferred phylogenetic relationships. Since most phylogenomic studies contain data partitions (e.g., genes) with missing taxa and IC scores stem from the frequencies of bipartitions (or splits) on a set of trees, the calculation of IC scores requires adjusting the frequencies of bipartitions from these partial gene trees. However, when the proportion of missing data is high, current approaches that adjust bipartition frequencies in partial gene trees tend to overestimate IC scores and alternative adjustment approaches differ substantially from each other in their scores. To overcome these issues, we developed three new measures for calculating internode certainty that are based on the frequencies of quartets, which naturally apply to both comprehensive and partial trees. Our comparison of these new quartet-based measures to previous bipartition-based measures on simulated data shows that: 1) on comprehensive trees, both types of measures yield highly similar IC scores; 2) on partial trees, quartet-based measures generate more accurate IC scores; and 3) quartet-based measures are more robust to the absence of phylogenetic signal and errors in the phylogenetic relationships to be assessed. Additionally, analysis of 15 empirical phylogenomic data sets using our quartet-based measures suggests that numerous relationships remain unresolved despite the availability of genome-scale data. Finally, we provide an efficient open-source implementation of these quartet-based measures in the program QuartetScores, which is freely available at https://github.com/algomaus/QuartetScores.

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Non-parametric correction of estimated gene trees using TRACTION

Algorithms for Molecular Biology ◽

10.1186/s13015-019-0161-8 ◽

2020 ◽

Vol 15 (1) ◽

Author(s):

Sarah Christensen ◽

Erin K. Molloy ◽

Pranjal Vachaspati ◽

Ananya Yammanuru ◽

Tandy Warnow

Keyword(s):

Incomplete Lineage Sorting ◽

Phylogenetic Signal ◽

Estimation Error ◽

Single Gene ◽

Gene Tree ◽

Species Tree ◽

Computational Techniques ◽

Gene Trees ◽

Species Trees ◽

Sequencing Data

Abstract Motivation Estimated gene trees are often inaccurate, due to insufficient phylogenetic signal in the single gene alignment, among other causes. Gene tree correction aims to improve the accuracy of an estimated gene tree by using computational techniques along with auxiliary information, such as a reference species tree or sequencing data. However, gene trees and species trees can differ as a result of gene duplication and loss (GDL), incomplete lineage sorting (ILS), and other biological processes. Thus gene tree correction methods need to take estimation error as well as gene tree heterogeneity into account. Many prior gene tree correction methods have been developed for the case where GDL is present. Results Here, we study the problem of gene tree correction where gene tree heterogeneity is instead due to ILS and/or HGT. We introduce TRACTION, a simple polynomial time method that provably finds an optimal solution to the RF-optimal tree refinement and completion (RF-OTRC) Problem, which seeks a refinement and completion of a singly-labeled gene tree with respect to a given singly-labeled species tree so as to minimize the Robinson−Foulds (RF) distance. Our extensive simulation study on 68,000 estimated gene trees shows that TRACTION matches or improves on the accuracy of well-established methods from the GDL literature when HGT and ILS are both present, and ties for best under the ILS-only conditions. Furthermore, TRACTION ties for fastest on these datasets. We also show that a naive generalization of the RF-OTRC problem to multi-labeled trees is possible, but can produce misleading results where gene tree heterogeneity is due to GDL.

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Quartet-Based Computations of Internode Certainty Provide Robust Measures of Phylogenetic Incongruence

Systematic Biology ◽

10.1093/sysbio/syz058 ◽

2019 ◽

Vol 69 (2) ◽

pp. 308-324 ◽

Cited By ~ 7

Author(s):

Xiaofan Zhou ◽

Sarah Lutteropp ◽

Lucas Czech ◽

Alexandros Stamatakis ◽

Moritz Von Looz ◽

...

Keyword(s):

Phylogenetic Trees ◽

Phylogenetic Signal ◽

Simulated Data ◽

Data Sets ◽

Gene Trees ◽

Data Set ◽

Statistical Confidence ◽

Branch Support ◽

Robust Measures ◽

Genome Scale

Abstract Incongruence, or topological conflict, is prevalent in genome-scale data sets. Internode certainty (IC) and related measures were recently introduced to explicitly quantify the level of incongruence of a given internal branch among a set of phylogenetic trees and complement regular branch support measures (e.g., bootstrap, posterior probability) that instead assess the statistical confidence of inference. Since most phylogenomic studies contain data partitions (e.g., genes) with missing taxa and IC scores stem from the frequencies of bipartitions (or splits) on a set of trees, IC score calculation typically requires adjusting the frequencies of bipartitions from these partial gene trees. However, when the proportion of missing taxa is high, the scores yielded by current approaches that adjust bipartition frequencies in partial gene trees differ substantially from each other and tend to be overestimates. To overcome these issues, we developed three new IC measures based on the frequencies of quartets, which naturally apply to both complete and partial trees. Comparison of our new quartet-based measures to previous bipartition-based measures on simulated data shows that: (1) on complete data sets, both quartet-based and bipartition-based measures yield very similar IC scores; (2) IC scores of quartet-based measures on a given data set with and without missing taxa are more similar than the scores of bipartition-based measures; and (3) quartet-based measures are more robust to the absence of phylogenetic signal and errors in phylogenetic inference than bipartition-based measures. Additionally, the analysis of an empirical mammalian phylogenomic data set using our quartet-based measures reveals the presence of substantial levels of incongruence for numerous internal branches. An efficient open-source implementation of these quartet-based measures is freely available in the program QuartetScores (https://github.com/lutteropp/QuartetScores).

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The synergistic effect of concatenation in phylogenomics: the case in Pantoea

PeerJ ◽

10.7717/peerj.6698 ◽

2019 ◽

Vol 7 ◽

pp. e6698 ◽

Cited By ~ 2

Author(s):

Marike Palmer ◽

Stephanus N. Venter ◽

Alistair R. McTaggart ◽

Martin P.A. Coetzee ◽

Stephanie Van Wyk ◽

...

Keyword(s):

Synergistic Effect ◽

Incomplete Lineage Sorting ◽

Phylogenetic Signal ◽

Single Gene ◽

Gene Tree ◽

Routine Practice ◽

Gene Trees ◽

Evolutionary Processes ◽

Species Phylogeny ◽

The Impact

With the increased availability of genome sequences for bacteria, it has become routine practice to construct genome-based phylogenies. These phylogenies have formed the basis for various taxonomic decisions, especially for resolving problematic relationships between taxa. Despite the popularity of concatenating shared genes to obtain well-supported phylogenies, various issues regarding this combined-evidence approach have been raised. These include the introduction of phylogenetic error into datasets, as well as incongruence due to organism-level evolutionary processes, particularly horizontal gene transfer and incomplete lineage sorting. Because of the huge effect that this could have on phylogenies, we evaluated the impact of phylogenetic conflict caused by organism-level evolutionary processes on the established species phylogeny for Pantoea, a member of the Enterobacterales. We explored the presence and distribution of phylogenetic conflict at the gene partition and nucleotide levels, by identifying putative inter-lineage recombination events that might have contributed to such conflict. Furthermore, we determined whether smaller, randomly constructed datasets had sufficient signal to reconstruct the current species tree hypothesis or if they would be overshadowed by phylogenetic incongruence. We found that no individual gene tree was fully congruent with the species phylogeny of Pantoea, although many of the expected nodes were supported by various individual genes across the genome. Evidence of recombination was found across all lineages within Pantoea, and provides support for organism-level evolutionary processes as a potential source of phylogenetic conflict. The phylogenetic signal from at least 70 random genes recovered robust, well-supported phylogenies for the backbone and most species relationships of Pantoea, and was unaffected by phylogenetic conflict within the dataset. Furthermore, despite providing limited resolution among taxa at the level of single gene trees, concatenated analyses of genes that were identified as having no signal resulted in a phylogeny that resembled the species phylogeny of Pantoea. This distribution of signal and noise across the genome presents the ideal situation for phylogenetic inference, as the topology from a ≥70-gene concatenated species phylogeny is not driven by single genes, and our data suggests that this finding may also hold true for smaller datasets. We thus argue that, by using a concatenation-based approach in phylogenomics, one can obtain robust phylogenies due to the synergistic effect of the combined signal obtained from multiple genes.

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