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

Neumann, Johannes S.; Desalle, Rob; Narechania, Apurva; Schierwater, Bernd; Tessler, Michael

doi:10.1093/sysbio/syaa038

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

Journal Article · Wed May 27 00:00:00 EDT 2020 · Systematic Biology

DOI:https://doi.org/10.1093/sysbio/syaa038· OSTI ID:1816872

Neumann, Johannes S. ^[1]; Desalle, Rob ^[2]; Narechania, Apurva ^[3]; Schierwater, Bernd ^[4]; Tessler, Michael ^[2]

American Museum of Natural History, New York, NY (United States). Richard Gilder Graduate School. Division of Invertebrate Zoology. Sackler Inst. for Comparative Genomics; OSTI
American Museum of Natural History, New York, NY (United States). Division of Invertebrate Zoology. Sackler Inst. for Comparative Genomics
American Museum of Natural History, New York, NY (United States). Sackler Inst. for Comparative Genomics
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.

View Accepted Manuscript (DOE)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0014377

OSTI ID:: 1816872

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 (104)

Data from: Morphological characters can strongly influence early animal relationships inferred from phylogenomic data sets Neumann, Johannes S.; Desalle, Rob; Narechania, Apurva Dryad https://doi.org/10.5061/dryad.prr4xgxhf	dataset	January 2020
Challenges of comprehensive taxon sampling in comparative biology: Wrestling with rosids Folk, Ryan A.; Sun, Miao; Soltis, Pamela S. American Journal of Botany, Vol. 105, Issue 3 https://doi.org/10.1002/ajb2.1059	journal	March 2018
Estimating Character Weights during Tree Search Goloboff, P. Cladistics, Vol. 9, Issue 1 https://doi.org/10.1006/clad.1993.1003	journal	March 1993
Cladistic Analysis of Metazoan Relationships: A Reappraisal Backeljau, T. Cladistics, Vol. 9, Issue 2 https://doi.org/10.1006/clad.1993.1010	journal	June 1993
Phylogeny of the Metazoa Based on Morphological and 18S Ribosomal DNA Evidence Zrzavý, J. Cladistics, Vol. 14, Issue 3 https://doi.org/10.1006/clad.1998.0070	journal	September 1998
Assessing the Relative Contribution of Molecular and Morphological Characters in Simultaneous Analysis Trees Baker, Richard H.; Yu, Xiaobo; DeSalle, Rob Molecular Phylogenetics and Evolution, Vol. 9, Issue 3 https://doi.org/10.1006/mpev.1998.0519	journal	June 1998
Rare genomic changes as a tool for phylogenetics Rokas, Antonis; Holland, Peter W. H. Trends in Ecology & Evolution, Vol. 15, Issue 11 https://doi.org/10.1016/S0169-5347(00)01967-4	journal	November 2000
Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry Moroz, Leonid L.; Edwards, John R.; Puthanveettil, Sathyanarayanan V. Cell, Vol. 127, Issue 7 https://doi.org/10.1016/j.cell.2006.09.052	journal	December 2006
Bayesian Inference of the Metazoan Phylogeny Glenner, Henrik; Hansen, Anders J.; Sørensen, Martin V. Current Biology, Vol. 14, Issue 18 https://doi.org/10.1016/j.cub.2004.09.027	journal	September 2004
Phylogenomics Revives Traditional Views on Deep Animal Relationships Philippe, Hervé; Derelle, Romain; Lopez, Philippe Current Biology, Vol. 19, Issue 8 https://doi.org/10.1016/j.cub.2009.02.052	journal	April 2009
Morphological Phylogenetics in the Genomic Age Lee, Michael S. Y.; Palci, Alessandro Current Biology, Vol. 25, Issue 19 https://doi.org/10.1016/j.cub.2015.07.009	journal	October 2015
A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals Simion, Paul; Philippe, Hervé; Baurain, Denis Current Biology, Vol. 27, Issue 7 https://doi.org/10.1016/j.cub.2017.02.031	journal	April 2017
Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals Feuda, Roberto; Dohrmann, Martin; Pett, Walker Current Biology, Vol. 27, Issue 24 https://doi.org/10.1016/j.cub.2017.11.008	journal	December 2017
A new criterion and method for amino acid classification Kosiol, Carolin; Goldman, Nick; H. Buttimore, Nigel Journal of Theoretical Biology, Vol. 228, Issue 1 https://doi.org/10.1016/j.jtbi.2003.12.010	journal	May 2004
The influence of taxon sampling on Bayesian divergence time inference under scenarios of rate heterogeneity among lineages Soares, André E. R.; Schrago, Carlos G. Journal of Theoretical Biology, Vol. 364 https://doi.org/10.1016/j.jtbi.2014.09.004	journal	January 2015
The Microtubular Cytoskeleton of the Apusomonad Thecamonas, a Sister Lineage to the Opisthokonts Heiss, Aaron A.; Walker, Giselle; Simpson, Alastair G. B. Protist, Vol. 164, Issue 5 https://doi.org/10.1016/j.protis.2013.05.005	journal	September 2013
Post-molecular systematics and the future of phylogenetics Pyron, R. Alexander Trends in Ecology & Evolution, Vol. 30, Issue 7 https://doi.org/10.1016/j.tree.2015.04.016	journal	July 2015
An artifact caused by undersampling optimal trees in supermatrix analyses of locally sampled characters Simmons, Mark P.; Goloboff, Pablo A. Molecular Phylogenetics and Evolution, Vol. 69, Issue 1 https://doi.org/10.1016/j.ympev.2013.06.001	journal	October 2013
What are the roles of taxon sampling and model fit in tests of cyto-nuclear discordance using avian mitogenomic data? Tamashiro, Ryan A.; White, Noor D.; Braun, Michael J. Molecular Phylogenetics and Evolution, Vol. 130 https://doi.org/10.1016/j.ympev.2018.10.008	journal	January 2019
Phylogenetic systematics turns over a new leaf Lewis, Paul O. Trends in Ecology & Evolution, Vol. 16, Issue 1 https://doi.org/10.1016/s0169-5347(00)02025-5	journal	January 2001
Counting mutations by parsimony and estimation of mutation rate variation across nucleotide sites —a simulation study Hong-Wen, Deng; Yun-Xin, Fu Mathematical and Computer Modelling, Vol. 32, Issue 1-2 https://doi.org/10.1016/s0895-7177(00)00121-7	journal	July 2000
Genome-scale approaches to resolving incongruence in molecular phylogenies Rokas, Antonis; Williams, Barry L.; King, Nicole Nature, Vol. 425, Issue 6960 https://doi.org/10.1038/nature02053	journal	October 2003
Broad phylogenomic sampling improves resolution of the animal tree of life Dunn, Casey W.; Hejnol, Andreas; Matus, David Q. Nature, Vol. 452, Issue 7188 https://doi.org/10.1038/nature06614	journal	March 2008
The Trichoplax genome and the nature of placozoans Srivastava, Mansi; Begovic, Emina; Chapman, Jarrod Nature, Vol. 454, Issue 7207 https://doi.org/10.1038/nature07191	journal	August 2008
The ctenophore genome and the evolutionary origins of neural systems Moroz, Leonid L.; Kocot, Kevin M.; Citarella, Mathew R. Nature, Vol. 510, Issue 7503 https://doi.org/10.1038/nature13400	journal	May 2014
Rare and low-frequency coding variants alter human adult height Marouli, Eirini; Graff, Mariaelisa; Medina-Gomez, Carolina Nature, Vol. 542, Issue 7640 https://doi.org/10.1038/nature21039	journal	February 2017
Causes of evolutionary rate variation among protein sites Echave, Julian; Spielman, Stephanie J.; Wilke, Claus O. Nature Reviews Genetics, Vol. 17, Issue 2 https://doi.org/10.1038/nrg.2015.18	journal	January 2016
Determinants of the rate of protein sequence evolution Zhang, Jianzhi; Yang, Jian-Rong Nature Reviews Genetics, Vol. 16, Issue 7 https://doi.org/10.1038/nrg3950	journal	June 2015
Model selection may not be a mandatory step for phylogeny reconstruction Abadi, Shiran; Azouri, Dana; Pupko, Tal Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08822-w	journal	February 2019
Contentious relationships in phylogenomic studies can be driven by a handful of genes Shen, Xing-Xing; Hittinger, Chris Todd; Rokas, Antonis Nature Ecology & Evolution, Vol. 1, Issue 5 https://doi.org/10.1038/s41559-017-0126	journal	April 2017
Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences Peterson, Kevin J.; Eernisse, Douglas J. Evolution and Development, Vol. 3, Issue 3 https://doi.org/10.1046/j.1525-142x.2001.003003170.x	journal	May 2001
Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum Dellaporta, S. L.; Xu, A.; Sagasser, S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 23 https://doi.org/10.1073/pnas.0602076103	journal	May 2006
Error, signal, and the placement of Ctenophora sister to all other animals Whelan, Nathan V.; Kocot, Kevin M.; Moroz, Leonid L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 18 https://doi.org/10.1073/pnas.1503453112	journal	April 2015
Genomic insights into the evolutionary origin of Myxozoa within Cnidaria Chang, E. Sally; Neuhof, Moran; Rubinstein, Nimrod D. Proceedings of the National Academy of Sciences, Vol. 112, Issue 48 https://doi.org/10.1073/pnas.1511468112	journal	November 2015
Incomplete taxon sampling is not a problem for phylogenetic inference Rosenberg, M. S.; Kumar, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 19 https://doi.org/10.1073/pnas.191248498	journal	August 2001
Rapid evolution of animal mitochondrial DNA. Brown, W. M.; George, M.; Wilson, A. C. Proceedings of the National Academy of Sciences, Vol. 76, Issue 4 https://doi.org/10.1073/pnas.76.4.1967	journal	April 1979
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 Buckley, Thomas R.; Simon, Chris; Chambers, Geoffrey K. Systematic Biology, Vol. 50, Issue 1 https://doi.org/10.1080/10635150116786	journal	February 2001
A Likelihood Approach to Estimating Phylogeny from Discrete Morphological Character Data Lewis, Paul O. Systematic Biology, Vol. 50, Issue 6 https://doi.org/10.1080/106351501753462876	journal	November 2001
Increased Taxon Sampling Greatly Reduces Phylogenetic Error Zwickl, Derrick J.; Hillis, David M. Systematic Biology, Vol. 51, Issue 4 https://doi.org/10.1080/10635150290102339	journal	July 2002
Increased Taxon Sampling Is Advantageous for Phylogenetic Inference Pollock, David D.; Zwickl, Derrick J.; McGuire, Jimmy A. Systematic Biology, Vol. 51, Issue 4 https://doi.org/10.1080/10635150290102357	journal	July 2002
Mosaics of Convergences and Noise in Morphological Phylogenies: What's in a Viverrid-Like Carnivoran? Gaubert, Philippe; Wozencraft, W. Chris; Cordeiro-Estrela, Pedro Systematic Biology, Vol. 54, Issue 6 https://doi.org/10.1080/10635150500232769	journal	December 2005
The Effect of Combining Molecular and Morphological Data in Published Phylogenetic Analyses Wortley, Alexandra H.; Scotland, Robert W. Systematic Biology, Vol. 55, Issue 4 https://doi.org/10.1080/10635150600899798	journal	August 2006
The impact of taxon sampling on phylogenetic inference: a review of two decades of controversy Nabhan, A. R.; Sarkar, I. N. Briefings in Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1093/bib/bbr014	journal	March 2011
Empirical profile mixture models for phylogenetic reconstruction Si Quang, Le; Gascuel, Olivier; Lartillot, Nicolas Bioinformatics, Vol. 24, Issue 20 https://doi.org/10.1093/bioinformatics/btn445	journal	August 2008
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
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 Narechania, Apurva; Baker, Richard H.; Sit, Ryan Genome Biology and Evolution, Vol. 4, Issue 1 https://doi.org/10.1093/gbe/evr121	journal	November 2011
Unleashing the Force of Cladistics? Metazoan Phylogenetics and Hypothesis Testing Jenner, R. A. Integrative and Comparative Biology, Vol. 43, Issue 1 https://doi.org/10.1093/icb/43.1.207	journal	February 2003
Placozoa Are Not Derived Cnidarians: Evidence from Molecular Morphology Ender, Andrea; Schierwater, Bernd Molecular Biology and Evolution, Vol. 20, Issue 1 https://doi.org/10.1093/molbev/msg018	journal	January 2003
More Genes or More Taxa? The Relative Contribution of Gene Number and Taxon Number to Phylogenetic Accuracy Rokas, Antonis; Carroll, Sean B. Molecular Biology and Evolution, Vol. 22, Issue 5 https://doi.org/10.1093/molbev/msi121	journal	March 2005
On Reduced Amino Acid Alphabets for Phylogenetic Inference Susko, E.; Roger, A. J. Molecular Biology and Evolution, Vol. 24, Issue 9 https://doi.org/10.1093/molbev/msm144	journal	May 2007
Near Intron Positions Are Reliable Phylogenetic Markers: An Application to Holometabolous Insects Krauss, Veiko; Thümmler, Christian; Georgi, Franziska Molecular Biology and Evolution, Vol. 25, Issue 5 https://doi.org/10.1093/molbev/msn013	journal	February 2008
Improved Phylogenomic Taxon Sampling Noticeably Affects Nonbilaterian Relationships Pick, K. S.; Philippe, H.; Schreiber, F. Molecular Biology and Evolution, Vol. 27, Issue 9 https://doi.org/10.1093/molbev/msq089	journal	April 2010
Choosing among Partition Models in Bayesian Phylogenetics Fan, Y.; Wu, R.; Chen, M. -H. Molecular Biology and Evolution, Vol. 28, Issue 1 https://doi.org/10.1093/molbev/msq224	journal	August 2010
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
New Statistical Criteria Detect Phylogenetic Bias Caused by Compositional Heterogeneity Duchêne, David A.; Duchêne, Sebastian; Ho, Simon Y. W. Molecular Biology and Evolution, Vol. 34, Issue 6 https://doi.org/10.1093/molbev/msx092	journal	February 2017
Uninformative Characters and Apparent Conflict Between Molecules and Morphology Lee, Michael S. Y. Molecular Biology and Evolution, Vol. 18, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a003848	journal	April 2001
Weighting, Partitioning, and Combining Characters in Phylogenetic Analysis Chippindale, P. T.; Wiens, J. J. Systematic Biology, Vol. 43, Issue 2 https://doi.org/10.1093/sysbio/43.2.278	journal	June 1994
Improving Marginal Likelihood Estimation for Bayesian Phylogenetic Model Selection Xie, Wangang; Lewis, Paul O.; Fan, Yu Systematic Biology, Vol. 60, Issue 2 https://doi.org/10.1093/sysbio/syq085	journal	December 2010
Detection of Implausible Phylogenetic Inferences Using Posterior Predictive Assessment of Model Fit Brown, Jeremy M. Systematic Biology, Vol. 63, Issue 3 https://doi.org/10.1093/sysbio/syu002	journal	February 2014
How Should Genes and Taxa be Sampled for Phylogenomic Analyses with Missing Data? An Empirical Study in Iguanian Lizards Streicher, Jeffrey W.; Schulte, James A.; Wiens, John J. Systematic Biology, Vol. 65, Issue 1 https://doi.org/10.1093/sysbio/syv058	journal	September 2015
Why Do Phylogenomic Data Sets Yield Conflicting Trees? Data Type Influences the Avian Tree of Life more than Taxon Sampling Reddy, Sushma; Kimball, Rebecca T.; Pandey, Akanksha Systematic Biology, Vol. 66, Issue 5 https://doi.org/10.1093/sysbio/syx041	journal	March 2017
Optimal Rates for Phylogenetic Inference and Experimental Design in the Era of Genome-Scale Data Sets Dornburg, Alex; Su, Zhuo; Townsend, Jeffrey P. Systematic Biology, Vol. 68, Issue 1 https://doi.org/10.1093/sysbio/syy047	journal	June 2018
Marginal Likelihoods in Phylogenetics: A Review of Methods and Applications R. Oaks, Jamie; A. Cobb, Kerry; N. Minin, Vladimir Systematic Biology, Vol. 68, Issue 5 https://doi.org/10.1093/sysbio/syz003	journal	January 2019
Combined morphological and phylogenomic re-examination of malawimonads, a critical taxon for inferring the evolutionary history of eukaryotes Heiss, Aaron A.; Kolisko, Martin; Ekelund, Fleming Royal Society Open Science, Vol. 5, Issue 4 https://doi.org/10.1098/rsos.171707	journal	April 2018
Early animal evolution: a morphologist's view Nielsen, Claus Royal Society Open Science, Vol. 6, Issue 7 https://doi.org/10.1098/rsos.190638	journal	July 2019
Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data Puttick, Mark N.; O'Reilly, Joseph E.; Tanner, Alastair R. Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1846 https://doi.org/10.1098/rspb.2016.2290	journal	January 2017
Deep conservation of cis -regulatory elements in metazoans Maeso, Ignacio; Irimia, Manuel; Tena, Juan J. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1632 https://doi.org/10.1098/rstb.2013.0020	journal	December 2013
Mutation rate variability as a driving force in adaptive evolution Engelhardt, Dalit; Shakhnovich, Eugene I. Physical Review E, Vol. 99, Issue 2 https://doi.org/10.1103/PhysRevE.99.022424	journal	February 2019
Extended implied weighting Goloboff, Pablo A. Cladistics, Vol. 30, Issue 3 https://doi.org/10.1111/cla.12047	journal	July 2013
Combined phylogeny of ray-finned fishes (Actinopterygii) and the use of morphological characters in large-scale analyses Mirande, Juan Marcos Cladistics, Vol. 33, Issue 4 https://doi.org/10.1111/cla.12171	journal	August 2016
Morphology, molecules and the phylogeny of Characidae (Teleostei, Characiformes) Mirande, Juan Marcos Cladistics, Vol. 35, Issue 3 https://doi.org/10.1111/cla.12345	journal	June 2018
PASOS: a method for the phylogenetic analysis of shape ontogenies Catalano, Santiago A.; Segura, Valentina; Vera Candioti, Florencia Cladistics, Vol. 35, Issue 6 https://doi.org/10.1111/cla.12373	journal	January 2019
Sampling diverse characters improves phylogenies: Craniodental and postcranial characters of vertebrates often imply different trees: HOMOPLASY IN VERTEBRATES Mounce, Ross C. P.; Sansom, Robert; Wills, Matthew A. Evolution, Vol. 70, Issue 3 https://doi.org/10.1111/evo.12884	journal	March 2016
The scientific status of metazoan cladistics: why current research practice must change Jenner, Ronald A. Zoologica Scripta, Vol. 33, Issue 4 https://doi.org/10.1111/j.0300-3256.2004.00153.x	journal	July 2004
On Simultaneous Analysis Nixon, Kevin C.; Carpenter, James M. Cladistics, Vol. 12, Issue 3 https://doi.org/10.1111/j.1096-0031.1996.tb00010.x	journal	September 1996
A review of long-branch attraction Bergsten, Johannes Cladistics, Vol. 21, Issue 2 https://doi.org/10.1111/j.1096-0031.2005.00059.x	journal	April 2005
Weighting against homoplasy improves phylogenetic analysis of morphological data sets Goloboff, Pablo A.; Carpenter, James M.; Arias, J. Salvador Cladistics, Vol. 24, Issue 5 https://doi.org/10.1111/j.1096-0031.2008.00209.x	journal	October 2008
TNT, a free program for phylogenetic analysis Goloboff, Pablo A.; Farris, James S.; Nixon, Kevin C. Cladistics, Vol. 24, Issue 5 https://doi.org/10.1111/j.1096-0031.2008.00217.x	journal	October 2008
A new dimension in combining data? The use of morphology and phylogenomic data in metazoan systematics Giribet, Gonzalo Acta Zoologica, Vol. 91, Issue 1 https://doi.org/10.1111/j.1463-6395.2009.00420.x	journal	January 2010
Deconstructing morphology Scholtz, Gerhard Acta Zoologica, Vol. 91, Issue 1 https://doi.org/10.1111/j.1463-6395.2009.00424.x	journal	January 2010
Description of a soft-bodied invertebrate with microcomputed tomography and revision of the genus Chtonobdella (Hirudinea: Haemadipsidae) Tessler, Michael; Barrio, Amalie; Borda, Elizabeth Zoologica Scripta, Vol. 45, Issue 5 https://doi.org/10.1111/zsc.12165	journal	January 2016
The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution Ryan, J. F.; Pang, K.; Schnitzler, C. E. Science, Vol. 342, Issue 6164 https://doi.org/10.1126/science.1242592	journal	December 2013
Molecular phylogeny of the animal kingdom Field, K.; Olsen, G.; Lane, D. Science, Vol. 239, Issue 4841 https://doi.org/10.1126/science.3277277	journal	February 1988
How natural selection affects mouse coat color Zahn, Laura M. Science, Vol. 363, Issue 6426 https://doi.org/10.1126/science.363.6426.494-i	journal	January 2019
Evolution of flower color pattern through selection on regulatory small RNAs Bradley, Desmond; Xu, Ping; Mohorianu, Irina-Ioana Science, Vol. 358, Issue 6365 https://doi.org/10.1126/science.aao3526	journal	November 2017
Molecular Versus Morphological Approaches To Systematics Hillis, D. Annual Review of Ecology and Systematics, Vol. 18, Issue 1 https://doi.org/10.1146/annurev.ecolsys.18.1.23	journal	January 1987
On the Independent Origins of Complex Brains and Neurons Moroz, Leonid L. Brain, Behavior and Evolution, Vol. 74, Issue 3 https://doi.org/10.1159/000258665	journal	January 2009
Different evolutionary pathways underlie the morphology of wrist bones in hominoids Kivell, Tracy L.; Barros, Anna P.; Smaers, Jeroen B. BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-229	journal	January 2013
Heterotachy and long-branch attraction in phylogenetics Philippe, Hervé; Zhou, Yan; Brinkmann, Henner BMC Evolutionary Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1471-2148-5-50	journal	October 2005
Convergent evolution of neural systems in ctenophores Moroz, Leonid L. Journal of Experimental Biology, Vol. 218, Issue 4 https://doi.org/10.1242/jeb.110692	journal	February 2015
Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis Schierwater, Bernd; Eitel, Michael; Jakob, Wolfgang PLoS Biology, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pbio.1000020	journal	January 2009
Comparative genomics and the nature of placozoan species Eitel, Michael; Francis, Warren R.; Varoqueaux, Frédérique PLOS Biology, Vol. 16, Issue 7 https://doi.org/10.1371/journal.pbio.2005359	journal	July 2018
Comparative Genomics of Large Mitochondria in Placozoans Signorovitch, Ana Y.; Buss, Leo W.; Dellaporta, Stephen L. PLoS Genetics, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pgen.0030013	journal	January 2007
Agent of Whirling Disease Meets Orphan Worm: Phylogenomic Analyses Firmly Place Myxozoa in Cnidaria Nesnidal, Maximilian P.; Helmkampf, Martin; Bruchhaus, Iris PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054576	journal	January 2013
Secondary Structure Analyses of the Nuclear rRNA Internal Transcribed Spacers and Assessment of Its Phylogenetic Utility across the Brassicaceae (Mustards) Edger, Patrick P.; Tang, Michelle; Bird, Kevin A. PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0101341	journal	July 2014
A Successive Approximations Approach to Character Weighting Farris, James S. Systematic Zoology, Vol. 18, Issue 4 https://doi.org/10.2307/2412182	journal	December 1969
Cases in which Parsimony or Compatibility Methods Will be Positively Misleading Felsenstein, Joseph Systematic Zoology, Vol. 27, Issue 4 https://doi.org/10.2307/2412923	journal	December 1978
Character Weighting and Cladistic Analysis Wheeler, Quentin D. Systematic Zoology, Vol. 35, Issue 1 https://doi.org/10.2307/2413294	journal	March 1986
A Concern for Evidence and a Phylogenetic Hypothesis of Relationships Among Epicrates (Boidae, Serpentes) Kluge, Arnold G. Systematic Zoology, Vol. 38, Issue 1 https://doi.org/10.2307/2992432	journal	March 1989
MtDNA The small workhorse of evolutionary studies Desalle, Rob Frontiers in Bioscience, Vol. 22, Issue 5 https://doi.org/10.2741/4522	journal	January 2017
Morphology is dead â€“ long live morphology! Integrating MorphoEvoDevo into molecular EvoDevo and phylogenomics Wanninger, Andreas Frontiers in Ecology and Evolution, Vol. 3 https://doi.org/10.3389/fevo.2015.00054	journal	May 2015
Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell Schierwater, Bernd; Holland, Peter W. H.; Miller, David J. Frontiers in Ecology and Evolution, Vol. 4 https://doi.org/10.3389/fevo.2016.00005	journal	February 2016
As Time Goes by: A Simple Fool's Guide to Molecular Clock Approaches in Invertebrates ^* Wilke, Thomas; Schultheiß, Roland; Albrecht, Christian American Malacological Bulletin, Vol. 27, Issue 1-2 https://doi.org/10.4003/006.027.0203	journal	July 2009
Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias Laumer, Christopher E.; Gruber-Vodicka, Harald; Hadfield, Michael G. eLife, Vol. 7 https://doi.org/10.7554/elife.36278	journal	October 2018

Cited By (1)

Data from: Morphological characters can strongly influence early animal relationships inferred from phylogenomic data sets Neumann, Johannes S.; Desalle, Rob; Narechania, Apurva Dryad https://doi.org/10.5061/dryad.prr4xgxhf	dataset	January 2020

Similar Records

Phylogenomics and the first higher taxonomy of Placozoa, an ancient and enigmatic animal phylum

Journal Article · Wed Dec 07 23:00:00 EST 2022 · Frontiers in Ecology and Evolution · OSTI ID:1902587

Functional phylogenomics analysis of bacteria and archaea using consistent genome annotation with UniFam

Journal Article · Thu Oct 09 00:00:00 EDT 2014 · BMC Evolutionary Biology (Online) · OSTI ID:1286772

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Metazoa
Morphology
Phylogenomics
Weighting

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

Citation Formats

References (104)

Cited By (1)

Similar Records

Related Subjects