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Title: Morphological Characters Can Strongly Influence Early Animal Relationships Inferred from Phylogenomic Data Sets

Journal Article · · Systematic Biology
 [1];  [2];  [3];  [4];  [2]
  1. American Museum of Natural History, New York, NY (United States). Richard Gilder Graduate School. Division of Invertebrate Zoology. Sackler Inst. for Comparative Genomics
  2. American Museum of Natural History, New York, NY (United States). Division of Invertebrate Zoology. Sackler Inst. for Comparative Genomics
  3. American Museum of Natural History, New York, NY (United States). Sackler Inst. for Comparative Genomics
  4. American Museum of Natural History, New York, NY (United States). Division of Invertebrate Zoology. Sackler Inst. for Comparative Genomics; Tierärztliche Hochschule Hannover (Germany). Division of Ecology and Evolution. ITZ

There are considerable phylogenetic incongruencies between morphological and phylogenomic data for the deep evolution of animals. This has contributed to a heated debate over the earliest-branching lineage of the animal kingdom: the sister to all other Metazoa (SOM). Here, we use published phylogenomic data sets ($$\sim $$45,000–400,000 characters in size with $$\sim $$15–100 taxa) that focus on early metazoan phylogeny to evaluate the impact of incorporating morphological data sets ($$\sim $$15–275 characters). We additionally use small exemplar data sets to quantify how increased taxon sampling can help stabilize phylogenetic inferences. We apply a plethora of common methods, that is, likelihood models and their “equivalent” under parsimony: character weighting schemes. Our results are at odds with the typical view of phylogenomics, that is, that genomic-scale data sets will swamp out inferences from morphological data. Instead, weighting morphological data 2–10$$\times $$ in both likelihood and parsimony can in some cases “flip” which phylum is inferred to be the SOM. This typically results in the molecular hypothesis of Ctenophora as the SOM flipping to Porifera (or occasionally Placozoa). However, greater taxon sampling improves phylogenetic stability, with some of the larger molecular data sets ($>$200,000 characters and up to $$\sim $$100 taxa) showing node stability even with $$\geqq100\times $$ upweighting of morphological data. Accordingly, our analyses have three strong messages. 1) The assumption that genomic data will automatically “swamp out” morphological data is not always true for the SOM question. Morphological data have a strong influence in our analyses of combined data sets, even when outnumbered thousands of times by molecular data. Morphology therefore should not be counted out a priori. 2) We here quantify for the first time how the stability of the SOM node improves for several genomic data sets when the taxon sampling is increased. 3) The patterns of “flipping points” (i.e., the weighting of morphological data it takes to change the inferred SOM) carry information about the phylogenetic stability of matrices. The weighting space is an innovative way to assess comparability of data sets that could be developed into a new sensitivity analysis tool.

Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0014377
OSTI ID:
1816872
Journal Information:
Systematic Biology, Vol. 70, Issue 2; ISSN 1063-5157
Publisher:
Society of Systematic Biologists - Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (103)

Mosaics of Convergences and Noise in Morphological Phylogenies: What's in a Viverrid-Like Carnivoran? journal December 2005
How natural selection affects mouse coat color journal January 2019
Agent of Whirling Disease Meets Orphan Worm: Phylogenomic Analyses Firmly Place Myxozoa in Cnidaria journal January 2013
As Time Goes by: A Simple Fool's Guide to Molecular Clock Approaches in Invertebrates * journal July 2009
Weighting against homoplasy improves phylogenetic analysis of morphological data sets journal October 2008
Weighting, Partitioning, and Combining Characters in Phylogenetic Analysis journal June 1994
Deconstructing morphology journal January 2010
Bayesian Inference of the Metazoan Phylogeny journal September 2004
A new dimension in combining data? The use of morphology and phylogenomic data in metazoan systematics journal January 2010
Comparative genomics and the nature of placozoan species journal July 2018
The Effect of Combining Molecular and Morphological Data in Published Phylogenetic Analyses journal August 2006
A Concern for Evidence and a Phylogenetic Hypothesis of Relationships Among Epicrates (Boidae, Serpentes) journal March 1989
Marginal Likelihoods in Phylogenetics: A Review of Methods and Applications journal January 2019
The influence of taxon sampling on Bayesian divergence time inference under scenarios of rate heterogeneity among lineages journal January 2015
Increased Taxon Sampling Greatly Reduces Phylogenetic Error journal July 2002
A new criterion and method for amino acid classification journal May 2004
Description of a soft-bodied invertebrate with microcomputed tomography and revision of the genus Chtonobdella (Hirudinea: Haemadipsidae) journal January 2016
The impact of taxon sampling on phylogenetic inference: a review of two decades of controversy journal March 2011
Genome-scale approaches to resolving incongruence in molecular phylogenies journal October 2003
Morphology, molecules and the phylogeny of Characidae (Teleostei, Characiformes) journal June 2018
Broad phylogenomic sampling improves resolution of the animal tree of life journal March 2008
On Simultaneous Analysis journal September 1996
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
PASOS: a method for the phylogenetic analysis of shape ontogenies journal January 2019
Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry journal December 2006
Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis journal January 2009
A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals journal April 2017
On the Independent Origins of Complex Brains and Neurons journal January 2009
Secondary Structure Analyses of the Nuclear rRNA Internal Transcribed Spacers and Assessment of Its Phylogenetic Utility across the Brassicaceae (Mustards) journal July 2014
Post-molecular systematics and the future of phylogenetics journal July 2015
Phylogenetic systematics turns over a new leaf journal January 2001
A review of long-branch attraction journal April 2005
Causes of evolutionary rate variation among protein sites journal January 2016
Deep conservation of cis -regulatory elements in metazoans journal December 2013
Unleashing the Force of Cladistics? Metazoan Phylogenetics and Hypothesis Testing journal February 2003
The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution journal December 2013
Uninformative Characters and Apparent Conflict Between Molecules and Morphology journal April 2001
Exploring Among-Site Rate Variation Models in a Maximum Likelihood Framework Using Empirical Data: Effects of Model Assumptions on Estimates of Topology, Branch Lengths, and Bootstrap Support journal February 2001
Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum journal May 2006
Improving Marginal Likelihood Estimation for Bayesian Phylogenetic Model Selection journal December 2010
Placozoa Are Not Derived Cnidarians: Evidence from Molecular Morphology journal January 2003
TNT, a free program for phylogenetic analysis journal October 2008
Convergent evolution of neural systems in ctenophores journal February 2015
Increased Taxon Sampling Is Advantageous for Phylogenetic Inference journal July 2002
MtDNA The small workhorse of evolutionary studies journal January 2017
Morphology is dead – long live morphology! Integrating MorphoEvoDevo into molecular EvoDevo and phylogenomics journal May 2015
Why Do Phylogenomic Data Sets Yield Conflicting Trees? Data Type Influences the Avian Tree of Life more than Taxon Sampling journal March 2017
Combined morphological and phylogenomic re-examination of malawimonads, a critical taxon for inferring the evolutionary history of eukaryotes journal April 2018
Morphological Phylogenetics in the Genomic Age journal October 2015
The scientific status of metazoan cladistics: why current research practice must change journal July 2004
The ctenophore genome and the evolutionary origins of neural systems journal May 2014
Sampling diverse characters improves phylogenies: Craniodental and postcranial characters of vertebrates often imply different trees: HOMOPLASY IN VERTEBRATES journal March 2016
What are the roles of taxon sampling and model fit in tests of cyto-nuclear discordance using avian mitogenomic data? journal January 2019
Determinants of the rate of protein sequence evolution journal June 2015
Different evolutionary pathways underlie the morphology of wrist bones in hominoids journal January 2013
Early animal evolution: a morphologist's view journal July 2019
New Statistical Criteria Detect Phylogenetic Bias Caused by Compositional Heterogeneity journal February 2017
Comparative Genomics of Large Mitochondria in Placozoans journal January 2007
Character Weighting and Cladistic Analysis journal March 1986
Random Addition Concatenation Analysis: A Novel Approach to the Exploration of Phylogenomic Signal Reveals Strong Agreement between Core and Shell Genomic Partitions in the Cyanobacteria journal November 2011
Choosing among Partition Models in Bayesian Phylogenetics journal August 2010
On Reduced Amino Acid Alphabets for Phylogenetic Inference journal May 2007
Contentious relationships in phylogenomic studies can be driven by a handful of genes journal April 2017
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
Rare and low-frequency coding variants alter human adult height journal February 2017
Cases in which Parsimony or Compatibility Methods Will be Positively Misleading journal December 1978
Phylogeny of the Metazoa Based on Morphological and 18S Ribosomal DNA Evidence journal September 1998
An artifact caused by undersampling optimal trees in supermatrix analyses of locally sampled characters journal October 2013
Combined phylogeny of ray-finned fishes (Actinopterygii) and the use of morphological characters in large-scale analyses journal August 2016
Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data journal January 2017
Mutation rate variability as a driving force in adaptive evolution journal February 2019
Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias journal October 2018
Challenges of comprehensive taxon sampling in comparative biology: Wrestling with rosids journal March 2018
The Trichoplax genome and the nature of placozoans journal August 2008
Empirical profile mixture models for phylogenetic reconstruction journal August 2008
Model selection may not be a mandatory step for phylogeny reconstruction journal February 2019
The Microtubular Cytoskeleton of the Apusomonad Thecamonas, a Sister Lineage to the Opisthokonts journal September 2013
Cladistic Analysis of Metazoan Relationships: A Reappraisal journal June 1993
Genomic insights into the evolutionary origin of Myxozoa within Cnidaria journal November 2015
Evolution of flower color pattern through selection on regulatory small RNAs journal November 2017
A Likelihood Approach to Estimating Phylogeny from Discrete Morphological Character Data journal November 2001
Error, signal, and the placement of Ctenophora sister to all other animals journal April 2015
Extended implied weighting journal July 2013
Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences journal May 2001
How Should Genes and Taxa be Sampled for Phylogenomic Analyses with Missing Data? An Empirical Study in Iguanian Lizards journal September 2015
Detection of Implausible Phylogenetic Inferences Using Posterior Predictive Assessment of Model Fit journal February 2014
Rapid evolution of animal mitochondrial DNA. journal April 1979
Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell journal February 2016
Optimal Rates for Phylogenetic Inference and Experimental Design in the Era of Genome-Scale Data Sets journal June 2018
Counting mutations by parsimony and estimation of mutation rate variation across nucleotide sites —a simulation study journal July 2000
A Successive Approximations Approach to Character Weighting journal December 1969
Incomplete taxon sampling is not a problem for phylogenetic inference journal August 2001
Assessing the Relative Contribution of Molecular and Morphological Characters in Simultaneous Analysis Trees journal June 1998
Improved Phylogenomic Taxon Sampling Noticeably Affects Nonbilaterian Relationships journal April 2010
Molecular Versus Morphological Approaches To Systematics journal January 1987
Near Intron Positions Are Reliable Phylogenetic Markers: An Application to Holometabolous Insects journal February 2008
Molecular phylogeny of the animal kingdom journal February 1988
Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals journal December 2017
More Genes or More Taxa? The Relative Contribution of Gene Number and Taxon Number to Phylogenetic Accuracy journal March 2005
Estimating Character Weights during Tree Search journal March 1993
Phylogenomics Revives Traditional Views on Deep Animal Relationships journal April 2009
Heterotachy and long-branch attraction in phylogenetics journal October 2005
Data from: Morphological characters can strongly influence early animal relationships inferred from phylogenomic data sets dataset January 2020

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