Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria

Journal Article · · Systematic Biology

Prokaryotic genomes are often considered to be mosaics of genes that do not necessarily share the same evolutionary history due to widespread horizontal gene transfers (HGTs). Consequently, representing evolutionary relationships of prokaryotes as bifurcating trees has long been controversial. However, studies reporting conflicts among gene trees derived from phylogenomic data sets have shown that these conflicts can be the result of artifacts or evolutionary processes other than HGT, such as incomplete lineage sorting, low phylogenetic signal, and systematic errors due to substitution model misspecification. Here, we present the results of an extensive exploration of phylogenetic conflicts in the cyanobacterial order Nostocales, for which previous studies have inferred strongly supported conflicting relationships when using different concatenated phylogenomic data sets. We found that most of these conflicts are concentrated in deep clusters of short internodes of the Nostocales phylogeny, where the great majority of individual genes have low resolving power. We then inferred phylogenetic networks to detect HGT events while also accounting for incomplete lineage sorting. Our results indicate that most conflicts among gene trees are likely due to incomplete lineage sorting linked to an ancient rapid radiation, rather than to HGTs. Moreover, the short internodes of this radiation fit the expectations of the anomaly zone, i.e., a region of the tree parameter space where a species tree is discordant with its most likely gene tree. In this work, we demonstrated that concatenation of different sets of loci can recover up to 17 distinct and well-supported relationships within the putative anomaly zone of Nostocales, corresponding to the observed conflicts among well-supported trees based on concatenated data sets from previous studies. Our findings highlight the important role of rapid radiations as a potential cause of strongly conflicting phylogenetic relationships when using phylogenomic data sets of bacteria. We propose that polytomies may be the most appropriate phylogenetic representation of these rapid radiations that are part of anomaly zones, especially when all possible genomic markers have been considered to infer these phylogenies.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE; National Science Foundation (NSF)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1972571
Journal Information:
Systematic Biology, Journal Name: Systematic Biology Journal Issue: 3 Vol. 72; ISSN 1063-5157
Publisher:
Society of Systematic Biologists - Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (134)

Data for: Ancient rapid radiation explains most conflicts among gene trees and well-supported phylogenomic trees of nostocalean cyanobacteria dataset January 2022
Data for: Ancient rapid radiation explains most conflicts among gene trees and well-supported phylogenomic trees of nostocalean cyanobacteria other January 2023
Specialized bacteriome uncovered in the coralloid roots of the epiphytic gymnosperm, Zamia pseudoparasitica journal January 2020
Defining the Core of Nontransferable Prokaryotic Genes: The Euryarchaeal Core journal October 2001
Geological constraints on the origin of oxygenic photosynthesis journal September 2010
UBCG2: Up-to-date bacterial core genes and pipeline for phylogenomic analysis journal May 2021
Comparison of phylogenetic trees journal February 1981
Patterns of speciation and limits to phylogenetic resolution journal March 1994
Archaeal genomics: Do archaea have a mixed heritage? journal March 1998
Lateral genomics journal December 1999
Elevated rates of horizontal gene transfer in the industrialized human microbiome journal April 2021
A Neoproterozoic Transition in the Marine Nitrogen Cycle journal March 2014
Cyanobacteria evolution: Insight from the fossil record journal August 2019
A renaissance for the pioneering 16S rRNA gene journal October 2008
The All-Species Living Tree project: A 16S rRNA-based phylogenetic tree of all sequenced type strains journal September 2008
The prokaryotic tree of life: past, present…and future? journal May 2008
DiscoVista: Interpretable visualizations of gene tree discordance journal May 2018
RAD sequencing resolves the phylogeny, taxonomy and biogeography of Trichophoreae despite a recent rapid radiation (Cyperaceae) journal April 2020
Exploring syntenic conservation across genomes for phylogenetic studies of organisms subjected to horizontal gene transfers: A case study with Cyanobacteria and cyanolichens journal September 2021
Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima journal May 1999
A comparison of homologous recombination rates in bacteria and archaea journal October 2008
Dating the rise of atmospheric oxygen journal January 2004
Inferring ancient divergences requires genes with strong phylogenetic signals journal May 2013
ModelFinder: fast model selection for accurate phylogenetic estimates journal May 2017
Microbial biogeography: putting microorganisms on the map journal February 2006
Coherence of Microcystis species revealed through population genomics journal July 2019
The rates of global bacterial and archaeal dispersal journal July 2021
Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea journal December 2019
Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding journal March 2021
Contentious relationships in phylogenomic studies can be driven by a handful of genes journal April 2017
Genome-wide analysis of the Firmicutes illuminates the diderm/monoderm transition journal October 2020
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life journal September 2017
A New Phylogenomic Approach For Quantifying Horizontal Gene Transfer Trends in Prokaryotes journal July 2020
Origin of marine planktonic cyanobacteria journal December 2015
The evolutionary diversification of cyanobacteria: Molecular-phylogenetic and paleontological perspectives journal March 2006
Genome evolution in cyanobacteria: The stable core and the variable shell journal February 2008
Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing journal December 2012
Horizontal gene transfer: A critical view journal August 2003
Ancient Yersinia pestis genomes from across Western Europe reveal early diversification during the First Pandemic (541–750) journal June 2019
Global-level population genomics reveals differential effects of geography and phylogeny on horizontal gene transfer in soil bacteria journal July 2019
Phylogenetic structure of the prokaryotic domain: The primary kingdoms journal November 1977
Molecular archaeology of the Escherichia coli genome journal August 1998
Inconsistency of Phylogenetic Estimates from Concatenated Data under Coalescence journal February 2007
Discordance of Species Trees with Their Most Likely Gene Trees: The Case of Five Taxa journal February 2008
More Characters or More Taxa for a Robust Phylogeny—Case Study from the Coffee Family (Rubiaceae) journal July 1999
Assessing the fit of the multi-species network coalescent to multi-locus data journal December 2020
APE: Analyses of Phylogenetics and Evolution in R language journal January 2004
Empirical profile mixture models for phylogenetic reconstruction journal August 2008
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating journal June 2009
The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell journal May 2010
BUCKy: Gene tree/species tree reconciliation with Bayesian concordance analysis journal September 2010
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs journal June 2015
Taxonomic Uncertainty and the Anomaly Zone: Phylogenomics Disentangle a Rapid Radiation to Resolve Contentious Species (Gila robustaComplex) in the Colorado River journal August 2021
To Tree or Not to Tree? Genome-Wide Quantification of Recombination and Reticulate Evolution during the Diversification of Strict Intracellular Bacteria journal November 2013
Cycad Coralloid Roots Contain Bacterial Communities Including Cyanobacteria and Caulobacter spp. That Encode Niche-Specific Biosynthetic Gene Clusters journal December 2018
Complete Genomes of Symbiotic Cyanobacteria Clarify the Evolution of Vanadium-Nitrogenase journal June 2019
Assessing the Impact of Secondary Structure and Solvent Accessibility on Protein Evolution journal May 1998
ASTRAL-Pro: Quartet-Based Species-Tree Inference despite Paralogy journal September 2020
Phylogenetic Analysis of SARS-CoV-2 Data Is Difficult journal December 2020
Extensive Genome-Wide Phylogenetic Discordance Is Due to Incomplete Lineage Sorting and Not Ongoing Introgression in a Rapidly Radiated Bryophyte Genus journal March 2021
Rooting the Animal Tree of Life journal June 2021
Weighting by Gene Tree Uncertainty Improves Accuracy of Quartet-based Species Trees journal October 2022
A Bayesian Mixture Model for Across-Site Heterogeneities in the Amino-Acid Replacement Process journal June 2004
More Genes or More Taxa? The Relative Contribution of Gene Number and Taxon Number to Phylogenetic Accuracy journal March 2005
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
Approximate Likelihood Calculation on a Phylogeny for Bayesian Estimation of Divergence Times journal February 2011
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
Discordance of Species Trees with Their Most Likely Gene Trees: A Unifying Principle journal September 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
Coalescent Methods Are Robust to the Simultaneous Effects of Long Branches and Incomplete Lineage Sorting journal November 2014
PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses journal December 2016
PhyloNetworks: A Package for Phylogenetic Networks journal September 2017
UFBoot2: Improving the Ultrafast Bootstrap Approximation journal October 2017
Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont journal March 2018
MAFFT version 5: improvement in accuracy of multiple sequence alignment journal January 2005
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments journal July 2006
OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs journal November 2018
Exploration of Plastid Phylogenomic Conflict Yields New Insights into the Deep Relationships of Leguminosae journal February 2020
Disentangling Sources of Gene Tree Discordance in Phylogenomic Data Sets: Testing Ancient Hybridizations in Amaranthaceae s.l journal June 2020
Gene Tree Estimation Error with Ultraconserved Elements: An Empirical Study on Pseudapis Bees journal December 2020
Phylogenomic Discordance in the Eared Seals is best explained by Incomplete Lineage Sorting following Explosive Radiation in the Southern Hemisphere journal December 2020
The Asymptotic Behavior of Bootstrap Support Values in Molecular Phylogenetics journal December 2020
Dissecting Incongruence between Concatenation- and Quartet-Based Approaches in Phylogenomic Data journal February 2021
What Is the Danger of the Anomaly Zone for Empirical Phylogenetics? journal August 2009
Sources of Error Inherent in Species-Tree Estimation: Impact of Mutational and Coalescent Effects on Accuracy and Implications for Choosing among Different Methods journal September 2010
Current Methods for Automated Filtering of Multiple Sequence Alignments Frequently Worsen Single-Gene Phylogenetic Inference journal June 2015
Exploring Tree-Like and Non-Tree-Like Patterns Using Genome Sequences: An Example Using the Inbreeding Plant Species Arabidopsis thaliana (L.) Heynh journal June 2015
The Phylogeny of Rickettsia Using Different Evolutionary Signatures: How Tree-Like is Bacterial Evolution? journal November 2015
Detecting the Anomaly Zone in Species Trees and Evidence for a Misleading Signal in Higher-Level Skink Phylogeny (Squamata: Scincidae). journal January 2016
Estimating Bayesian Phylogenetic Information Content journal May 2016
Phylogenomic Systematics of Ostariophysan Fishes: Ultraconserved Elements Support the Surprising Non-Monophyly of Characiformes journal February 2017
Why Concatenation Fails Near the Anomaly Zone journal July 2017
Modeling Site Heterogeneity with Posterior Mean Site Frequency Profiles Accelerates Accurate Phylogenomic Estimation journal August 2017
The Past Sure is Tense: On Interpreting Phylogenetic Divergence Time Estimates journal September 2017
Variation Across Mitochondrial Gene Trees Provides Evidence for Systematic Error: How Much Gene Tree Variation Is Biological? journal February 2018
Phylogenomic Analysis of the Explosive Adaptive Radiation of the Espeletia Complex (Asteraceae) in the Tropical Andes journal March 2018
Evaluating Statistical Multiple Sequence Alignment in Comparison to Other Alignment Methods on Protein Data Sets journal October 2018
Resolving Deep Nodes in an Ancient Radiation of Neotropical Fishes in the Presence of Conflicting Signals from Incomplete Lineage Sorting journal December 2018
Whole-Genome Analyses Resolve the Phylogeny of Flightless Birds (Palaeognathae) in the Presence of an Empirical Anomaly Zone journal April 2019
The Relative Importance of Modeling Site Pattern Heterogeneity Versus Partition-Wise Heterotachy in Phylogenomic Inference journal April 2019
Phylogenomics Uncovers Confidence and Conflict in the Rapid Radiation of Australo-Papuan Rodents journal September 2019
How big is the iceberg of which organellar genes in nuclear genomes are but the tip?
  • Doolittle, W. F.; Boucher, Y.; NesbØ, C. L.
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 358, Issue 1429 https://doi.org/10.1098/rstb.2002.1185
journal January 2003
Phylogenetic mixture models for proteins journal October 2008
A Phylogenomic Approach to Bacterial Phylogeny: Evidence of a Core of Genes Sharing a Common History journal July 2002
metaSPAdes: a new versatile metagenomic assembler journal March 2017
Phylogenetic analyses of cyanobacterial genomes: Quantification of horizontal gene transfer events journal August 2006
Irrational exuberance for resolved species trees: COMMENTARY journal December 2015
Genome-Wide Experimental Determination of Barriers to Horizontal Gene Transfer journal November 2007
Phylogenetic Classification and the Universal Tree journal June 1999
A rooted phylogeny resolves early bacterial evolution journal May 2021
16S rRNA Gene Sequencing for Bacterial Identification in the Diagnostic Laboratory: Pluses, Perils, and Pitfalls journal July 2007
Metagenome Sequencing to Explore Phylogenomics of Terrestrial Cyanobacteria journal June 2021
T-BAS Version 2.1: Tree-Based Alignment Selector Toolkit for Evolutionary Placement of DNA Sequences and Viewing Alignments and Specimen Metadata on Curated and Custom Trees journal July 2019
Cyanocohniella calida gen. et sp. nov. (Cyanobacteria: Aphanizomenonaceae) a new cyanobacterium from the thermal springs from Karlovy Vary, Czech Republic journal October 2014
High-throughput genome sequencing of lichenizing fungi to assess gene loss in the ammonium transporter/ammonia permease gene family journal January 2013
A simple, fast, and accurate method of phylogenomic inference journal January 2008
ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees journal May 2018
Analysis of phylogenomic datasets reveals conflict, concordance, and gene duplications with examples from animals and plants journal August 2015
TreeShrink: fast and accurate detection of outlier long branches in collections of phylogenetic trees journal May 2018
Distinctive characters of Nostoc genomes in cyanolichens journal June 2018
Genotyping and phylogenetic placement of Bacillus anthracis isolates from Finland, a country with rare anthrax cases journal September 2018
GUNC: detection of chimerism and contamination in prokaryotic genomes journal June 2021
Resolving Difficult Phylogenetic Questions: Why More Sequences Are Not Enough journal March 2011
ClipKIT: A multiple sequence alignment trimming software for accurate phylogenomic inference journal December 2020
Discordance of Species Trees with Their Most Likely Gene Trees journal May 2006
Inferring Phylogenetic Networks with Maximum Pseudolikelihood under Incomplete Lineage Sorting journal March 2016
Comparison of French and Worldwide Bacillus anthracis Strains Favors a Recent, Post-Columbian Origin of the Predominant North-American Clade journal February 2016
A Comprehensive Study of Cyanobacterial Morphological and Ecological Evolutionary Dynamics through Deep Geologic Time journal September 2016
Insights from Bacillus anthracis strains isolated from permafrost in the tundra zone of Russia journal May 2019
Polytomies and the Power of Phylogenetic Inference journal June 1999
Ecogenomics and Taxonomy of Cyanobacteria Phylum journal November 2017
AMAS: a fast tool for alignment manipulation and computing of summary statistics journal January 2016

Similar Records

Disentangling Sources of Gene Tree Discordance in Phylogenomic Data Sets: Testing Ancient Hybridizations in Amaranthaceae s.l
Journal Article · Fri Jun 12 00:00:00 EDT 2020 · Systematic Biology · OSTI ID:1851159

A genome-scale phylogeny of the kingdom Fungi
Journal Article · Wed Feb 17 23:00:00 EST 2021 · Current Biology · OSTI ID:1804876

Extensive Genome-Wide Phylogenetic Discordance Is Due to Incomplete Lineage Sorting and Not Ongoing Introgression in a Rapidly Radiated Bryophyte Genus
Journal Article · Tue Mar 02 23:00:00 EST 2021 · Molecular Biology and Evolution (Online) · OSTI ID:1815542