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

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

Journal Article · · Systematic Biology
 [1];  [2];  [2];  [3];  [4];  [5];  [5];  [6];  [6];  [7]
  1. Univ. of Minnesota, Twin Cities, St. Paul, MN (United States); OSTI
  2. Johannes Gutenberg Univ., Mainz (Germany)
  3. Oberlin College, OH (United States)
  4. Univ. of Michigan, Ann Arbor, MI (United States)
  5. Univ. of Cambridge (United Kingdom)
  6. Univ. of Nevada, Reno, NV (United States)
  7. Univ. of Minnesota, Twin Cities, St. Paul, MN (United States)
Gene tree discordance in large genomic data sets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. that was previously supported by morphological, ecological, and Sanger-based molecular data. The data set included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations.
Research Organization:
University of Nevada, Reno, NV (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE Office of Science (SC); University of Michigan; University of Minnesota
Grant/Contract Number:
SC0008834
OSTI ID:
1851159
Journal Information:
Systematic Biology, Journal Name: Systematic Biology Journal Issue: 2 Vol. 70; ISSN 1063-5157
Publisher:
Society of Systematic Biologists - Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (118)

Disentangling sources of gene tree discordance in phylogenomic datasets: testing ancient hybridizations in Amaranthaceae s.l. dataset January 2020
Quartet Sampling distinguishes lack of support from conflicting support in the green plant tree of life journal February 2018
A matter of phylogenetic scale: Distinguishing incomplete lineage sorting from lateral gene transfer as the cause of gene tree discord in recent versus deep diversification histories journal March 2018
From cacti to carnivores: Improved phylotranscriptomic sampling and hierarchical homology inference provide further insight into the evolution of Caryophyllales journal March 2018
Phylogeny of Polycnemoideae (Amaranthaceae): Implications for biogeography, character evolution and taxonomy journal February 2013
An evolutionary perspective on synonymous codon usage in unicellular organisms journal December 1986
Halophyte Halogeton glomeratus, a promising candidate for phytoremediation of heavy metal-contaminated saline soils journal July 2019
The Phylogenetic Association Between Salt Tolerance and Heavy Metal Hyperaccumulation in Angiosperms journal November 2015
Comparison of phylogenetic trees journal February 1981
Evolutionary ecology of fast seed germination—A case study in Amaranthaceae/Chenopodiaceae journal December 2017
Overly simplistic substitution models obscure green plant phylogeny journal September 2014
Gene tree discordance, phylogenetic inference and the multispecies coalescent journal June 2009
Implementing and testing the multispecies coalescent model: A valuable paradigm for phylogenomics journal January 2016
Plastid phylogenomic insights into the evolution of Caryophyllales journal May 2019
Incongruence between gene trees and species trees and phylogenetic signal variation in plastid genes journal September 2019
The genome of the recently domesticated crop plant sugar beet (Beta vulgaris) journal December 2013
The genome of Chenopodium quinoa journal February 2017
Full-length transcriptome assembly from RNA-Seq data without a reference genome journal May 2011
Draft genome of spinach and transcriptome diversity of 120 Spinacia accessions journal May 2017
ModelFinder: fast model selection for accurate phylogenetic estimates journal May 2017
Comparative assessment shows the reliability of chloroplast genome assembly using RNA-seq journal November 2018
Multiple historical processes obscure phylogenetic relationships in a taxonomically difficult group (Lobariaceae, Ascomycota) journal June 2019
Full transcription of the chloroplast genome in photosynthetic eukaryotes journal July 2016
Maximum likelihood inference of reticulate evolutionary histories journal November 2014
Extensive gene tree discordance and hemiplasy shaped the genomes of North American columnar cacti journal October 2017
Network-based microsynteny analysis identifies major differences and genomic outliers in mammalian and angiosperm genomes journal January 2019
Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. journal July 1995
Further analysts of the data by akaike' s information criterion and the finite corrections: Further analysts of the data by akaike' s journal January 1978
Difficulties in Detecting Hybridization journal November 2001
An Approximately Unbiased Test of Phylogenetic Tree Selection journal May 2002
Modeling Compositional Heterogeneity journal June 2004
Differentiating between Hypotheses of Lineage Sorting and Introgression in New Zealand Alpine Cicadas (Maoricicada Dugdale) journal June 2006
The Reticulate History of Medicago (Fabaceae) journal June 2008
Phylogeny of Amaranthaceae and Chenopodiaceae and the Evolution of C 4 Photosynthesis journal November 2003
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing journal May 2012
Plant salt tolerance: adaptations in halophytes journal February 2015
Evolutionary diversification of the African achyranthoid clade (Amaranthaceae) in the context of sterile flower evolution and epizoochory journal April 2018
RNA-Seq data: a goldmine for organelle research journal January 2013
CONSEL: for assessing the confidence of phylogenetic tree selection journal December 2001
Phybase: an R package for species tree analysis journal February 2010
phangorn: phylogenetic analysis in R journal December 2010
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data journal April 2012
treePL: divergence time estimation using penalized likelihood for large phylogenies journal August 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
Quartet Inference from SNP Data Under the Coalescent Model journal August 2014
Phyx: phylogenetic tools for unix journal February 2017
A divide-and-conquer method for scalable phylogenetic network inference from multilocus data journal July 2019
Performance of gene expression analyses using de novo assembled transcripts in polyploid species journal August 2019
Macroclimatic niche limits and the evolution of C4 photosynthesis in Gomphrenoideae (Amaranthaceae) journal June 2017
Bayes Estimation of Species Divergence Times and Ancestral Population Sizes Using DNA Sequences From Multiple Loci journal August 2003
New Methods to Calculate Concordance Factors for Phylogenomic Datasets journal May 2020
Testing for Ancient Admixture between Closely Related Populations journal February 2011
Statistics and Truth in Phylogenomics journal August 2011
PartitionFinder: Combined Selection of Partitioning Schemes and Substitution Models for Phylogenetic Analyses journal January 2012
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
Novel Information Theory-Based Measures for Quantifying Incongruence among Phylogenetic Trees journal February 2014
Orthology Inference in Nonmodel Organisms Using Transcriptomes and Low-Coverage Genomes: Improving Accuracy and Matrix Occupancy for Phylogenomics journal August 2014
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
Fast Coalescent-Based Computation of Local Branch Support from Quartet Frequencies journal April 2016
TreeScaper: Visualizing and Extracting Phylogenetic Signal from Sets of Trees journal September 2016
UFBoot2: Improving the Ultrafast Bootstrap Approximation journal October 2017
The PREP suite: predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments journal May 2009
Gene Trees in Species Trees journal September 1997
What Is the Danger of the Anomaly Zone for Empirical Phylogenetics? journal August 2009
Conflicting Phylogenies for Early Land Plants are Caused by Composition Biases among Synonymous Substitutions journal January 2014
Mitochondrial Phylogenomics of Early Land Plants: Mitigating the Effects of Saturation, Compositional Heterogeneity, and Codon-Usage Bias journal July 2014
Evaluating Summary Methods for Multilocus Species Tree Estimation in the Presence of Incomplete Lineage Sorting journal August 2014
Detecting the Anomaly Zone in Species Trees and Evidence for a Misleading Signal in Higher-Level Skink Phylogeny (Squamata: Scincidae). journal January 2016
Inferring Phylogenetic Networks Using PhyloNet journal March 2018
Impacts of Inference Method and Data set Filtering on Phylogenomic Resolution in a Rapid Radiation of Ground Squirrels (Xerinae: Marmotini) journal September 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
Model Choice, Missing Data, and Taxon Sampling Impact Phylogenomic Inference of Deep Basidiomycota Relationships journal May 2019
Phylogenomics Uncovers Confidence and Conflict in the Rapid Radiation of Australo-Papuan Rodents journal September 2019
Phylogenetic Trees and Networks Can Serve as Powerful and Complementary Approaches for Analysis of Genomic Data journal September 2019
Quartet-Based Computations of Internode Certainty Provide Robust Measures of Phylogenetic Incongruence journal August 2019
A broader model for C 4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.) journal May 2012
Dealing with incongruence in phylogenomic analyses journal October 2008
An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV journal March 2016
DISCORDANCE BETWEEN NUCLEAR AND CHLOROPLAST PHYLOGENIES IN THE HEUCHERA GROUP (SAXIFRAGACEAE) journal August 1995
Is a new and General Theory of Molecular Systematics Emerging? journal January 2009
Reticulate evolutionary history and extensive introgression in mosquito species revealed by phylogenetic network analysis journal March 2016
Conflicting phylogenomic signals reveal a pattern of reticulate evolution in a recent high‐Andean diversification (Asteraceae: Astereae: Diplostephium ) journal March 2017
Phylogenomic analyses reveal a deep history of hybridization and polyploidy in the Neotropical genus Lachemilla (Rosaceae) journal March 2018
An evaluation of alternative explanations for widespread cytonuclear discordance in annual sunflowers ( Helianthus ) journal August 2018
Uncovering the genomic signature of ancient introgression between white oak lineages ( Quercus ) journal May 2019
Large‐scale genomic sequence data resolve the deepest divergences in the legume phylogeny and support a near‐simultaneous evolutionary origin of all six subfamilies journal December 2019
A Draft Sequence of the Neandertal Genome journal May 2010
Extensive introgression in a malaria vector species complex revealed by phylogenomics journal November 2014
Assorted angiosperm pollen from the Edmonton Formation (Maestrichtian), Alberta, Canada journal June 1969
Simulation-Based Evaluation of Hybridization Network Reconstruction Methods in the Presence of Incomplete Lineage Sorting journal January 2017
PhyloNet: a software package for analyzing and reconstructing reticulate evolutionary relationships journal July 2008
A maximum pseudo-likelihood approach for phylogenetic networks journal October 2015
A scalability study of phylogenetic network inference methods using empirical datasets and simulations involving a single reticulation journal October 2016
Gene flow analysis method, the D-statistic, is robust in a wide parameter space journal January 2018
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
An invariants-based method for efficient identification of hybrid species from large-scale genomic data journal May 2019
Single-molecule sequencing and Hi-C-based proximity-guided assembly of amaranth (Amaranthus hypochondriacus) chromosomes provide insights into genome evolution journal August 2017
Estimating the Dimension of a Model journal March 1978
Phylogeny, biogeography, systematics and taxonomy of Salicornioideae (Amaranthaceae/Chenopodiaceae) – A cosmopolitan, highly specialized hygrohalophyte lineage dating back to the Oligocene journal February 2017
Discordance of Species Trees with Their Most Likely Gene Trees journal May 2006
The Probability of a Gene Tree Topology within a Phylogenetic Network with Applications to Hybridization Detection journal April 2012
Inferring Phylogenetic Networks with Maximum Pseudolikelihood under Incomplete Lineage Sorting journal March 2016
A Simple and Robust Statistical Test for Detecting the Presence of Recombination journal February 2006
Challenges in Species Tree Estimation Under the Multispecies Coalescent Model journal December 2016
Phylogeny and Evolution of the Neotropical Radiation of Lachemilla (Rosaceae): Uncovering a History of Reticulate Evolution and Implications for Infrageneric Classification journal March 2018
Gene Trees and Species Trees: Molecular Systematics as One-Character Taxonomy journal January 1992
Understanding Mediterranean‐Californian disjunctions: molecular evidence from Chenopodiaceae‐Betoideae journal February 2006
A taxonomic backbone for the global synthesis of species diversity in the angiosperm order Caryophyllales journal September 2015
RNA-Seq Assembly – Are We There Yet? journal January 2012
An Efficient Field and Laboratory Workflow for Plant Phylotranscriptomic Projects journal March 2017
A scalability study of phylogenetic network inference methods using empirical datasets and simulations involving a single reticulation collection January 2016
Gene flow analysis method, the D-statistic, is robust in a wide parameter space collection January 2018
ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees collection January 2018
Characterizing gene tree conflict in plastome-inferred phylogenies journal January 2019
Network-based Microsynteny Analysis Identifies Major Differences and Genomic Outliers in Mammalian and Angiosperm Genomes dataset January 2018

Cited By (3)