Morphology's role in phylogeny reconstruction: perspectives from paleontology.

A recent article by Scotland et al. (2003; hereafter referred to as SEA) purporting to examine the value of morphological data in phylogeny reconstruction has been received critically by several systematists (Jenner, 2004; Wiens, 2004). As paleontologists—and in an area of systematics restricted solely to morphological data—we take exception to many of the arguments put forward by SEA and feel we may provide a unique perspective in the debate. In their paper, SEA argued for a redefined role for morphology in phylogeny reconstruction, one in which “rigorous and critical anatomical studies of fewer morphological characters, in the context of molecular phylogenies, is a more fruitful approach to integrating the strengths of morphological data with those of sequence data” (p. 539). Such a statement is bold and therefore warrants a critical analysis, as it would effectively neuter the ability of morphological data to generate novel phylogenies. Though issues such as accuracy, support, character coding, and character conceptualization were discussed by SEA, in all cases these discussions resorted to a “too few characters” argument. As the authors characterized it, the “main constraint of morphology-based phylogenetic inference concerns the limited number of unambiguous characters available for analysis in a transformational framework” (p. 539). Additionally, the merits of increased taxon sampling in the context of morphological data were discussed by SEA, and found to be lacking. Though several of the views presented by SEA are not novel (see Hedges and Sibley, 1994, and Hedges and Maxson, 1996), they provide the most detailed recent discussion of this position. We agree with many of the points made by SEA, especially the call for more critical and rigorous analysis of morphology; however, we draw different conclusions from the data. It is our goal to reexamine some of the arguments put forward by SEA, in order to illustrate that a much more optimistic conclusion exists regarding the current and future role of morphology in phylogeny reconstruction.

[1]  R. DeSalle,et al.  Assessing the relative contribution of molecular and morphological characters in simultaneous analysis trees. , 1998, Molecular phylogenetics and evolution.

[2]  J. Huelsenbeck,et al.  Hobgoblin of phylogenetics? , 1994, Nature.

[3]  D. Hillis,et al.  Taxonomic sampling, phylogenetic accuracy, and investigator bias. , 1998, Systematic biology.

[4]  D. Swofford,et al.  Taxon sampling revisited , 1999, Nature.

[5]  C. dePamphilis,et al.  Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Sudhir Kumar,et al.  Incomplete taxon sampling is not a problem for phylogenetic inference , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Miyamoto,et al.  Phylogenetic Analysis of DNA Sequences , 1991 .

[8]  M. Zelditch,et al.  Why morphometrics is not special: coding quantitative data for phylogenetic analysis. , 1998, Systematic biology.

[9]  K. Bremer THE LIMITS OF AMINO ACID SEQUENCE DATA IN ANGIOSPERM PHYLOGENETIC RECONSTRUCTION , 1988, Evolution; international journal of organic evolution.

[10]  Arnold G. Kluge,et al.  AMNIOTE PHYLOGENY AND THE IMPORTANCE OF FOSSILS , 1988, Cladistics : the international journal of the Willi Hennig Society.

[11]  Mark W. Chase,et al.  The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes , 1999, Nature.

[12]  H Philippe,et al.  Species sampling has a major impact on phylogenetic inference. , 1993, Molecular phylogenetics and evolution.

[13]  F. Rohlf,et al.  EVALUATION OF THE RESTRICTED MAXIMUM‐LIKELIHOOD METHOD FOR ESTIMATING PHYLOGENETIC TREES USING SIMULATED ALLELE‐FREQUENCY DATA , 1988, Evolution; international journal of organic evolution.

[14]  G. Edgecombe,et al.  Arthropod Fossils and Phylogeny , 1999 .

[15]  P. D. Polly Paleophylogeography of Sorex araneus (Insectivora, Soricidae): molar shape as a morphological marker for fossil shrews , 2003 .

[16]  Michael J. Sanderson,et al.  THE RELATIONSHIP BETWEEN HOMOPLASY AND CONFIDENCE IN A PHYLOGENETIC TREE , 1996 .

[17]  P. Herendeen Review of: Systematics and the fossil record: documenting evolutionary patterns, Andrew B. Smith, 1994, Blackwell Scientific Publications: ASPT Newsletter , 1995 .

[18]  R. Olmstead,et al.  Phylogeny reconstruction: the role of morphology. , 2003, Systematic biology.

[19]  A. Smith,et al.  Systematics and the Fossil Record: Documenting Evolutionary Patterns , 1994 .

[20]  A B Smith,et al.  What does palaeontology contribute to systematics in a molecular world? , 1998, Molecular phylogenetics and evolution.

[21]  R. Ward,et al.  Complete mitochondrial genome sequences of two extinct moas clarify ratite evolution , 2001, Nature.

[22]  J. Levinton,et al.  SIMULATIONS OF EVOLUTIONARY RADIATIONS AND THEIR APPLICATION TO UNDERSTANDING THE PROBABILITY OF A CAMBRIAN EXPLOSION , 2004, Journal of Paleontology.

[23]  J. Bull,et al.  Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7. , 1997, Molecular biology and evolution.

[24]  Peter C. Hoch,et al.  A Phylogenetic Analysis of Epilobium (Onagraceae) Based on Nuclear Ribosomal DNA Sequences , 1994 .

[25]  J. Doyle Seed Plant Phylogeny and the Relationships of Gnetales , 1996, International Journal of Plant Sciences.

[26]  Junhyong Kim,et al.  ACCURACY OF PHYLOGENETIC‐ESTIMATION METHODS UNDER UNEQUAL EVOLUTIONARY RATES , 1988, Evolution; international journal of organic evolution.

[27]  J. Palmer,et al.  Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Doyle Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. , 1998, Molecular phylogenetics and evolution.

[29]  S. Carroll,et al.  Conflicting phylogenetic signals at the base of the metazoan tree , 2003, Evolution & development.

[30]  Yoshio Tateno,et al.  Accuracy of estimated phylogenetic trees from molecular data , 2005, Journal of Molecular Evolution.

[31]  H. Shaffer,et al.  Tests of turtle phylogeny: molecular, morphological, and paleontological approaches. , 1997, Systematic biology.

[32]  D. Hillis Inferring complex phytogenies , 1996, Nature.

[33]  John P. Huelsenbeck,et al.  WHEN ARE FOSSILS BETTER THAN EXTANT TAXA IN PHYLOGENETIC ANALYSIS , 1991 .

[34]  S. Hedges,et al.  Molecular evidence for the origin of birds. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Michael J. Sanderson,et al.  Homoplasy. The Recurrence of Similarity in Evolution. , 1997 .

[36]  Seed plant phylogeny , 2000 .

[37]  A. Graybeal,et al.  Is it better to add taxa or characters to a difficult phylogenetic problem? , 1998, Systematic biology.

[38]  D. Penny,et al.  The Use of Tree Comparison Metrics , 1985 .

[39]  S. Hedges,et al.  Re: Molecules and morphology in amniote phylogeny. , 1996, Molecular phylogenetics and evolution.

[40]  J. Gillespie The causes of molecular evolution , 1991 .

[41]  D A Morrison,et al.  Effects of nucleotide sequence alignment on phylogeny estimation: a case study of 18S rDNAs of apicomplexa. , 1997, Molecular biology and evolution.

[42]  J. Huelsenbeck,et al.  Application and accuracy of molecular phylogenies. , 1994, Science.

[43]  R. Olmstead,et al.  Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. , 2000, American journal of botany.

[44]  Hedges Sb,et al.  Re: Molecules and morphology in amniote phylogeny. , 1996 .

[45]  J. Huelsenbeck,et al.  SUCCESS OF PHYLOGENETIC METHODS IN THE FOUR-TAXON CASE , 1993 .

[46]  B. Bremer,et al.  More characters or more taxa for a robust phylogeny--case study from the coffee family (Rubiaceae). , 1999, Systematic biology.

[47]  S. Hedges,et al.  Molecules vs. morphology in avian evolution: the case of the "pelecaniform" birds. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[48]  S. Poe Sensitivity of phylogeny estimation to taxonomic sampling. , 1998, Systematic biology.

[49]  J. Wiens The role of morphological data in phylogeny reconstruction. , 2004, Systematic biology.

[50]  Nick Goldman,et al.  Effects of sequence alignment procedures on estimates of phylogeny , 1998 .

[51]  C. Darwin On the Origin of Species by Means of Natural Selection: Or, The Preservation of Favoured Races in the Struggle for Life , 2019 .

[52]  E. Ray Lankester,et al.  II.—On the use of the term homology in modern zoology, and the distinction between homogenetic and homoplastic agreements , 1870 .

[53]  G. Wagner The character concept in evolutionary biology , 2001 .

[54]  P. D. Polly PALEOPHYLOGEOGRAPHY OF SOREX ARANEUS : MOLAR SHAPE AS A MORPHOLOGICAL MARKER FOR FOSSIL SHREWS , 2003 .

[55]  M. Donoghue,et al.  The Importance of Fossils in Phylogeny Reconstruction , 1989 .

[56]  James Lyons-Weiler,et al.  Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  D. Robinson,et al.  Comparison of phylogenetic trees , 1981 .

[58]  Kevin C. Nixon,et al.  A Reevaluation of Seed Plant Phylogeny , 1994 .

[59]  Charles Darwin,et al.  The Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. New York (The Modern Library) 1998. , 1998 .

[60]  M. Donoghue,et al.  The root of angiosperm phylogeny inferred from duplicate phytochrome genes. , 1999, Science.

[61]  S. Poe Evaluation of the strategy of long-branch subdivision to improve the accuracy of phylogenetic methods. , 2003, Systematic biology.

[62]  D. Hillis Inferring complex phylogenies. , 1996, Nature.

[63]  M. Novacek,et al.  Extinction and phylogeny , 1992 .

[64]  M. Donoghue,et al.  PATTERNS OF VARIATION IN LEVELS OF HOMOPLASY , 1989, Evolution; international journal of organic evolution.

[65]  T. Givnish,et al.  Consistency, characters, and the likelihood of correct phylogenetic inference. , 1997, Molecular phylogenetics and evolution.

[66]  P. D. Polly PALEOPHYLOGEOGRAPHY: THE TEMPO OF GEOGRAPHIC DIFFERENTIATION IN MARMOTS (MARMOTA) , 2003 .

[67]  B. Lim,et al.  Distributional extension of Molossops neglectus (Chiroptera, Molossidae) into southeastern Brazil , 2004 .

[68]  B. Rannala,et al.  Taxon sampling and the accuracy of large phylogenies. , 1998, Systematic biology.

[69]  J. Bull,et al.  Exceptional convergent evolution in a virus. , 1997, Genetics.

[70]  Mark P. Simmons,et al.  Gaps as characters in sequence-based phylogenetic analyses. , 2000, Systematic biology.

[71]  M. Wills,et al.  An arthropod phylogeny based on fossil and recent taxa , 1998 .

[72]  M. Donoghue,et al.  The importance of fossils in elucidating seed plant phylogeny and macroevolution , 1987 .

[73]  D. Hillis,et al.  When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders. , 2003, Systematic biology.

[74]  Peter R. Crane,et al.  Phylogenetic analysis of seed plants and the origin of angiosperms , 1985 .

[75]  S. Hedges,et al.  Tetrapod phylogeny inferred from 18S and 28S ribosomal RNA sequences and a review of the evidence for amniote relationships. , 1990, Molecular biology and evolution.

[76]  R. Jenner,et al.  Accepting partnership by submission? Morphological phylogenetics in a molecular millennium. , 2004, Systematic biology.

[77]  Anne Chenuil,et al.  Can the Cambrian explosion be inferred through molecular phylogeny , 1994 .

[78]  P. Forey,et al.  Morphology, shape and phylogeny , 2002 .

[79]  MICHAEL A. CHARLESTON,et al.  The Effects of Sequence Length, Tree Topology, and Number of Taxa on the Performance of Phylogenetic Methods , 1994, J. Comput. Biol..

[80]  P. D. Polly On morphological clocks and paleophylogeography: towards a timescale for Sorex hybrid zones , 2004, Genetica.

[81]  D. Soltis,et al.  Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology , 1999, Nature.

[82]  M. Carine,et al.  Classification of Strobilanthinae (Acanthaceae): Trying to classify the unclassifiable? , 2002 .