A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): identification of localized incongruence using a combinational bootstrap approach.

Multi-gene phylogenetic analyses were conducted to address the evolution of Clavicipitaceae (Ascomycota). Data are presented here for approximately 5900 base pairs from portions of seven loci: the nuclear ribosomal small and large subunit DNA (nrSSU and nrLSU), beta-tubulin, elongation factor 1alpha (EF-1alpha), the largest and second largest subunits of RNA polymerase II (RPB1 and RPB2), and mitochondrial ATP Synthase subunit 6 (mtATP6). These data were analyzed in a complete 66-taxon matrix and 91-taxon supermatrix that included some missing data. Separate phylogenetic analyses, with data partitioned according to genes, produced some conflicting results. The results of separate analyses from RPB1 and RPB2 are in agreement with the combined analyses that resolve a paraphyletic Clavicipitaceae comprising three well-supported clades (i.e., Clavicipitaceae clade A, B, and C), whereas the tree obtained from mtATP6 is in strong conflict with the monophyly of Clavicipitaceae clade B and the sister-group relationship of Hypocreaceae and Clavicipitaceae clade C. The distribution of relative contribution of nodal support for each gene partition was assessed using both partitioned Bremer support (PBS) values and combinational bootstrap (CB) analyses, the latter of which analyzed bootstrap proportions from all possible combinations of the seven gene partitions. These results suggest that CB analyses provide a more consistent estimate of nodal support than PBS and that combining heterogeneous gene partitions, which individually support a limited number of nodes, results in increased support for overall tree topology. Analyses of the 91-taxa supermatrix data sets revealed that some nodes were more strongly supported by increased taxon sampling. Identifying the localized incongruence of mtATP6 and analyses of complete and supermatrix data sets strengthen the evidence for rejecting the monophyly of Clavicipitaceae and much of the current subfamilial classification of the family. Although the monophyly of the grass-associated subfamily Clavicipitoideae (e.g., Claviceps, Balansia, and Epichloë) is strongly supported, the subfamily Cordycipitoideae (e.g., Cordyceps and Torrubiella) is not monophyletic. In particular, species of the genus Cordyceps, which are pathogens of arthropods and truffles, are found in all three clavicipitaceous clades. These results imply that most characters used in the current familial classification of Clavicipitaceae are not diagnostic of monophyly.

[1]  Antonis Rokas,et al.  Comparing bootstrap and posterior probability values in the four-taxon case. , 2003, Systematic biology.

[2]  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.

[3]  R. Wayne,et al.  Type I STS markers are more informative than cytochrome B in phylogenetic reconstruction of the Mustelidae (Mammalia: Carnivora). , 2003, Systematic biology.

[4]  A. Rossman,et al.  Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes) , 1999 .

[5]  R. Baker,et al.  Corroboration among Data Sets in Simultaneous Analysis: Hidden Support for Phylogenetic Relationships among Higher Level Artiodactyl Taxa , 1999, Cladistics : the international journal of the Willi Hennig Society.

[6]  A. Kluge.  A Concern for Evidence and a Phylogenetic Hypothesis of Relationships among Epicrates (Boidae, Serpentes) , 1989 .

[7]  Y. Passamaneck,et al.  Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences. , 2004, Molecular phylogenetics and evolution.

[8]  J. Spatafora,et al.  Independent terrestrial origins of the Halosphaeriales (marine Ascomycota). , 1998, American journal of botany.

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

[10]  H. Shaffer,et al.  Multiple data sets, high homoplasy, and the phylogeny of softshell turtles (Testudines: Trionychidae). , 2004, Systematic biology.

[11]  J. C. Regier,et al.  More taxa or more characters revisited: combining data from nuclear protein-encoding genes for phylogenetic analyses of Noctuoidea (Insecta: Lepidoptera). , 2000, Systematic biology.

[12]  J. Stone,et al.  Phylogenetic analysis of nuclear ribosomal DNA places the nematode parasite, Drechmeria coniospora, in Clavicipitaceae , 1999 .

[13]  D. Hibbett,et al.  Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. , 2004, American journal of botany.

[14]  J. Wiens,et al.  INCOMPLETE TAXA, INCOMPLETE CHARACTERS, AND PHYLOGENETIC ACCURACY: IS THERE A MISSING DATA PROBLEM? , 2003 .

[15]  Charles W. Bacon,et al.  Molecular phylogeny of Acremonium and its taxonomic implications. , 1996 .

[16]  C. Rogerson.  The hypocrealean fungi (Ascomycetes, Hypocreales). , 1970, Mycologia.

[17]  M. Melkonian,et al.  Are combined analyses better than single gene phylogenies? A case study using SSU rDNA and rbcL sequence comparisons in the Zygnematophyceae (Streptophyta). , 2003, Molecular biology and evolution.

[18]  F. Kauff,et al.  Phylogeny of the Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. , 2002, Molecular phylogenetics and evolution.

[19]  M. Stanhope,et al.  Molecular phylogenetic evidence refuting the hypothesis of Batoidea (rays and skates) as derived sharks. , 2003, Molecular Phylogenetics and Evolution.

[20]  E. Braun,et al.  Examining Basal avian divergences with mitochondrial sequences: model complexity, taxon sampling, and sequence length. , 2002, Systematic biology.

[21]  R. DeSalle,et al.  A new method to localize and test the significance of incongruence: detecting domain shuffling in the nuclear receptor superfamily. , 2000, Systematic biology.

[22]  J. Spatafora,et al.  A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae , 2001 .

[23]  John J. Wiens,et al.  Weighting, Partitioning, and Combining Characters in Phylogenetic Analysis , 1994 .

[24]  Seán G. Brady,et al.  Single-copy nuclear genes recover cretaceous-age divergences in bees. , 2004, Systematic biology.

[25]  Emily C. Moriarty,et al.  The importance of proper model assumption in bayesian phylogenetics. , 2004, Systematic biology.

[26]  F. Lutzoni,et al.  Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. , 2004, Molecular phylogenetics and evolution.

[27]  J. Sullivan.  Combining Data with Different Distributions of Among-Site Rate Variation , 1996 .

[28]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[29]  F. K. Barker,et al.  The utility of the incongruence length difference test. , 2002, Systematic biology.

[30]  J. Wiens.  Combining data sets with different phylogenetic histories. , 1998, Systematic biology.

[31]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[32]  D. Winkler,et al.  Phylogeny of the tree swallow genus, Tachycineta (Aves: Hirundinidae), by Bayesian analysis of mitochondrial DNA sequences. , 2002, Molecular phylogenetics and evolution.

[33]  S. Rehner,et al.  Molecular systematics of the Hypocreales: a teleomorph gene phylogeny and the status of their anamorphs , 1995 .

[34]  G. Purschke,et al.  Phylogeny of Eunicida (Annelida) and exploring data congruence using a partition addition bootstrap alteration (PABA) approach. , 2006, Systematic biology.

[35]  M. Donoghue,et al.  Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. , 2001, Systematic biology.

[36]  Ichael,et al.  Analysis of Character Correlations Among Wood Decay Mechanisms , Mating Systems , and Substrate Ranges in Homobasidiomycetes , 2001 .

[37]  D. Maddison,et al.  MacClade 4: analysis of phy-logeny and character evolution , 2003 .

[38]  A. Austin,et al.  Increased congruence does not necessarily indicate increased phylogenetic accuracy--the behavior of the incongruence length difference test in mixed-model analyses. , 2002, Systematic biology.

[39]  J. Wiens,et al.  Missing data, incomplete taxa, and phylogenetic accuracy. , 2003, Systematic biology.

[40]  J. Spatafora.  The Molecular Systematics of Unitunicate, Perithecial Ascomycetes. , 1992 .

[41]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

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

[43]  Derrick J. Zwickl,et al.  Increased taxon sampling greatly reduces phylogenetic error. , 2002, Systematic biology.

[44]  P. Sundberg,et al.  Phylogeny and evolution of reproductive modes in Autolytinae (Syllidae, Annelida). , 2003, Molecular phylogenetics and evolution.

[45]  O. Eriksson,et al.  Neolecta—a fungal dinosaur? Evidence from β-tubulin amino acid sequences , 2001 .

[46]  F. Lutzoni,et al.  Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. , 2003, Molecular biology and evolution.

[47]  Ebecca,et al.  Points of View Examining Basal Avian Divergences with Mitochondrial Sequences: Model Complexity, Taxon Sampling, and Sequence Length , 2002 .

[48]  E. Gäumann.  Vergleichende Morphologie der Pilze , 1926 .

[49]  J. Spatafora,et al.  Multigene phylogeny reveals new lineage for Stachybotrys chartarum, the indoor air fungus. , 2004, Mycological research.

[50]  A. Kluge.  Total Evidence Or Taxonomic Congruence: Cladistics Or Consensus Classification , 1998, Cladistics : the international journal of the Willi Hennig Society.

[51]  B. Rannala,et al.  Phylogenetic methods come of age: testing hypotheses in an evolutionary context. , 1997, Science.

[52]  Odi,et al.  Failure of the ILD to Determine Data Combinability for Slow Loris Phylogeny , 2001 .

[53]  J. Bull,et al.  Partitioning and combining data in phylogenetic analysis , 1993 .

[54]  J. Spatafora,et al.  MOLECULAR SYSTEMATICS OF UNITUNICATE PERITHECIAL ASCOMYCETES: THE CLAVICIPITALES-HYPOCREALES CONNECTION , 1993 .

[55]  Michael M. Miyamoto,et al.  TESTING SPECIES PHYLOGENIES AND PHYLOGENETIC METHODS WITH CONGRUENCE , 1995 .

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

[57]  John P. Huelsenbeck,et al.  A Likelihood Ratio Test to Detect Conflicting Phylogenetic Signal , 1996 .

[58]  Bryan Kolaczkowski,et al.  Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous , 2004, Nature.

[59]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[60]  R DeSalle,et al.  Multiple sources of character information and the phylogeny of Hawaiian drosophilids. , 1997, Systematic biology.

[61]  T. Britton,et al.  Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. , 2003, Systematic biology.

[62]  M. Steel,et al.  Recovering evolutionary trees under a more realistic model of sequence evolution. , 1994, Molecular biology and evolution.

[63]  W. W. Diehl.  Balansia and the Balansiae in America. , 1950 .

[64]  K. O’Donnell,et al.  Generic classification of some more hyphomycetes with solitary conidia borne on phialides , 1998 .

[65]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[66]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[67]  S. Carroll,et al.  More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. , 2005, Molecular biology and evolution.

[68]  B. Larget,et al.  Markov Chain Monte Carlo Algorithms for the Bayesian Analysis of Phylogenetic Trees , 2000 .

[69]  A. Kluge,et al.  CLADISTICS: WHAT'S IN A WORD? , 1993, Cladistics : the international journal of the Willi Hennig Society.

[70]  K. Bremer,et al.  BRANCH SUPPORT AND TREE STABILITY , 1994 .

[71]  C. Orme,et al.  Noise and incongruence: interpreting results of the incongruence length difference test. , 2000, Molecular phylogenetics and evolution.

[72]  E. S. Luttrell.  The Ascostromatic Ascomycetes , 1955 .

[73]  A. Hipp,et al.  Congruence versus phylogenetic accuracy: revisiting the incongruence length difference test. , 2004, Systematic biology.

[74]  John McNeill,et al.  International Code of Botanical Nomenclature , 1983 .

[75]  H. Akaike.  A new look at the statistical model identification , 1974 .

[76]  H. Lumbsch,et al.  Outline of Ascomycota - 2007 , 2007 .

[77]  Masatoshi Nei,et al.  Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[78]  J. Spatafora,et al.  Clavicipitalean Fungi: evolutionary biology, chemistry, biocontrol and cultural impacts. , 2003 .

[79]  A. Queiroz.  For Consensus (Sometimes) , 1993 .

[80]  F. Lapointe,et al.  War and peace in phylogenetics: a rejoinder on total evidence and consensus. , 2001, Systematic biology.

[81]  W. Doolittle,et al.  Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. , 2003, Molecular biology and evolution.

[82]  E. Gareth Jones,et al.  Relationship of the genusCordyceps and related genera, based on parsimony and spectral analysis of partial 18S and 28S ribosomal gene sequences , 2001 .

[83]  C. Bult,et al.  TESTING SIGNIFICANCE OF INCONGRUENCE , 1994 .

[84]  Allen G. Rodrigo,et al.  A randomisation test of the null hypothesis that two cladograms are sample estimates of a parametric phylogenetic tree , 1993 .

[85]  J. Bull,et al.  An Empirical Test of Bootstrapping as a Method for Assessing Confidence in Phylogenetic Analysis , 1993 .

[86]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .