Mitochondrial genome data alone are not enough to unambiguously resolve the relationships of Entognatha, Insecta and Crustacea sensu lato (Arthropoda)

An analysis of the relationships of the major arthropod groups was undertaken using mitochondrial genome data to examine the hypotheses that Hexapoda is polyphyletic and that Collembola is more closely related to branchiopod crustaceans than insects. We sought to examine the sensitivity of this relationship to outgroup choice, data treatment, gene choice and optimality criteria used in the phylogenetic analysis of mitochondrial genome data. Additionally we sequenced the mitochondrial genome of an archaeognathan, Nesomachilis australica, to improve taxon selection in the apterygote insects, a group poorly represented in previous mitochondrial phylogenies. The sister group of the Collembola was rarely resolved in our analyses with a significant level of support. The use of different outgroups (myriapods, nematodes, or annelids + mollusks) resulted in many different placements of Collembola. The way in which the dataset was coded for analysis (DNA, DNA with the exclusion of third codon position and as amino acids) also had marked affects on tree topology. We found that nodal support was spread evenly throughout the 13 mitochondrial genes and the exclusion of genes resulted in significantly less resolution in the inferred trees. Optimality criteria had a much lesser effect on topology than the preceding factors; parsimony and Bayesian trees for a given data set and treatment were quite similar. We therefore conclude that the relationships of the extant arthropod groups as inferred by mitochondrial genomes are highly vulnerable to outgroup choice, data treatment and gene choice, and no consistent alternative hypothesis of Collembola's relationships is supported. Pending the resolution of these identified problems with the application of mitogenomic data to basal arthropod relationships, it is difficult to justify the rejection of hexapod monophyly, which is well supported on morphological grounds.

[1]  B. Jin,et al.  The mitochondrial genome of the firefly, Pyrocoelia rufa: complete DNA sequence, genome organization, and phylogenetic analysis with other insects. , 2004, Molecular phylogenetics and evolution.

[2]  Gonzalo Giribet Relationships among metazoan phyla as inferred from 18S rRNA sequence data: a methodological approach. , 2002, EXS.

[3]  M. Jackson,et al.  Origin of the Metazoa , 1979, Nature.

[4]  Jon E. Ahlquist,et al.  Phylogeny and Classification of the Birds: A Study in Molecular Evolution , 1991 .

[5]  A. Kurabayashi,et al.  Complete sequence of the mitochondrial DNA of the primitive opisthobranch gastropod Pupa strigosa: systematic implication of the genome organization. , 2000, Molecular biology and evolution.

[6]  C. Gissi,et al.  Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. , 1999, Gene.

[7]  James M. Carpenter,et al.  The Phylogeny of the Extant Hexapod Orders , 2001, Cladistics : the international journal of the Willi Hennig Society.

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

[9]  J. Cornuet,et al.  The complete sequence of the mitochondrial genome of the honeybee ectoparasite mite Varroa destructor (Acari: Mesostigmata). , 2002, Molecular biology and evolution.

[10]  Douglas O. Clary,et al.  The mitochondrial DNA molecule ofDrosophila yakuba: Nucleotide sequence, gene organization, and genetic code , 2005, Journal of Molecular Evolution.

[11]  T. Bourgoin,et al.  The phylogenetic position of early hexapod lineages: morphological data contradict molecular data , 2004 .

[12]  G. Valle,et al.  The mitochondrial genome of the house centipede scutigera and the monophyly versus paraphyly of myriapods. , 2004, Molecular biology and evolution.

[13]  J. Boore,et al.  Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. , 2000, Molecular biology and evolution.

[14]  T. Spears,et al.  Crustacean phylogeny inferred from 18S rDNA , 1998 .

[15]  S. Carranza,et al.  First molecular evidence for the existence of a Tardigrada + Arthropoda clade. , 1996, Molecular biology and evolution.

[16]  S. Pääbo,et al.  The mitochondrial genome of a monotreme—the platypus (Ornithrohynchus anatinus) , 1996, Journal of Molecular Evolution.

[17]  R. Okimoto,et al.  The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. , 1992, Genetics.

[18]  W. Wheeler,et al.  The position of arthropods in the animal kingdom: Ecdysozoa, islands, trees, and the "Parsimony ratchet". , 1999, Molecular phylogenetics and evolution.

[19]  R. Raff,et al.  Molecular phylogeny of the animal kingdom. , 1988, Science.

[20]  G. C. Rodakis,et al.  Complete sequence and gene organization of the mitochondrial genome of the land snail Albinaria coerulea. , 1995, Genetics.

[21]  M. S. Lee,et al.  Partitioned likelihood support and the evaluation of data set conflict. , 2003, Systematic biology.

[22]  Christian Hennig,et al.  Biotic element analysis in biogeography. , 2003, Systematic biology.

[23]  A. Kluge,et al.  Transformation Series as an Ideographic Character Concept , 2004, Cladistics : the international journal of the Willi Hennig Society.

[24]  Gonzalo Giribet,et al.  A Review of Arthropod Phylogeny: New Data Based on Ribosomal DNA Sequences and Direct Character Optimization , 2000 .

[25]  W. Black,et al.  Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. , 1998, Molecular biology and evolution.

[26]  C. D’Haese Morphological appraisal of Collembola phylogeny with special emphasis on Poduromorpha and a test of the aquatic origin hypothesis , 2003 .

[27]  M. Miya,et al.  Complete mitochondrial DNA sequence of the swimming crab, Portunus trituberculatus (Crustacea: Decapoda: Brachyura). , 2003, Gene.

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

[29]  D. M. Hamm,et al.  The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects , 1993, Insect molecular biology.

[30]  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.

[31]  A. Beckenbach,et al.  Phylogenetic and genomic analysis of the complete mitochondrial DNA sequence of the spotted asparagus beetle Crioceris duodecimpunctata. , 2003, Molecular phylogenetics and evolution.

[32]  C. Rowell,et al.  The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome , 1995, Journal of Molecular Evolution.

[33]  M. Miya,et al.  Complete mitochondrial DNA sequence of the Japanese spiny lobster, Panulirus japonicus (Crustacea: Decapoda). , 2002, Gene.

[34]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[35]  R. Shao,et al.  The mitochondrial genomes of soft ticks have an arrangement of genes that has remained unchanged for over 400 million years , 2004, Insect molecular biology.

[36]  M. Friedrich,et al.  Sequence and phylogenetic analysis of the complete mitochondrial genome of the flour beetle Tribolium castanaeum. , 2003, Molecular phylogenetics and evolution.

[37]  J. Boore,et al.  Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. , 1994, Genetics.

[38]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[39]  T. Oshima,et al.  The Cephalopod Loligo bleekeri Mitochondrial Genome: Multiplied Noncoding Regions and Transposition of tRNA Genes , 2002, Journal of Molecular Evolution.

[40]  A. Bezděk,et al.  Phylogeny of the Metazoa Based on Morphological and 18S Ribosomal DNA Evidence , 1998, Cladistics : the international journal of the Willi Hennig Society.

[41]  G. Edgecombe,et al.  Regular ArticleArthropod Cladistics: Combined Analysis of Histone H3 and U2 snRNA Sequences and Morphology☆ , 2000 .

[42]  C. Cunningham,et al.  Dramatic mitochondrial gene rearrangements in the hermit crab Pagurus longicarpus (Crustacea, anomura). , 2000, Molecular biology and evolution.

[43]  C. Ribera,et al.  A Review of Arthropod Phylogeny: New Data Based on Ribosomal DNA Sequences and Direct Character Optimization , 2000, Cladistics : the international journal of the Willi Hennig Society.

[44]  T. Unnasch,et al.  The mitochondrial genome of Onchocerca volvulus: sequence, structure and phylogenetic analysis. , 1998, Molecular and biochemical parasitology.

[45]  P. Arruda,et al.  The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera: Calliphoridae) , 2000, Insect molecular biology.

[46]  J. Benzie,et al.  The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? , 2000, Molecular biology and evolution.

[47]  Axel Janke,et al.  Phylogenetic Analysis of 18S rRNA and the Mitochondrial Genomes of the Wombat, Vombatus ursinus, and the Spiny Anteater, Tachyglossus aculeatus: Increased Support for the Marsupionta Hypothesis , 2002, Journal of Molecular Evolution.

[48]  R. Zardoya,et al.  The complete mitochondrial genome of the nudibranch Roboastra europaea (Mollusca: Gastropoda) supports the monophyly of opisthobranchs. , 2002, Molecular biology and evolution.

[49]  A. Cockburn,et al.  The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. , 1993, Genome.

[50]  M. Simmons,et al.  Conflict between Amino Acid and Nucleotide Characters , 2002 .

[51]  D. Penny,et al.  Comment on "Hexapod Origins: Monophyletic or Paraphyletic?" , 2003, Science.

[52]  Ward C. Wheeler,et al.  NUCLEIC ACID SEQUENCE PHYLOGENY AND RANDOM OUTGROUPS , 1990, Cladistics : the international journal of the Willi Hennig Society.

[53]  R. Shao,et al.  Numerous gene rearrangements in the mitochondrial genome of the wallaby louse, Heterodoxus macropus (Phthiraptera). , 2001, Molecular biology and evolution.

[54]  R. Shao,et al.  The highly rearranged mitochondrial genome of the plague thrips, Thrips imaginis (Insecta: Thysanoptera): convergence of two novel gene boundaries and an extraordinary arrangement of rRNA genes. , 2003, Molecular biology and evolution.

[55]  E. Dotson,et al.  Sequence and organization of the mitochondrial genome of the Chagas disease vector, Triatoma dimidiata , 2001, Insect molecular biology.

[56]  Gonzalo Giribet,et al.  Arthropod phylogeny based on eight molecular loci and morphology , 2001, Nature.

[57]  A Janke,et al.  The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupialia, and Eutheria. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Boore,et al.  A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[59]  R. Marco,et al.  Speciation in the Artemia genus: Mitochondrial DNA analysis of bisexual and parthenogenetic brine shrimps , 1994, Journal of Molecular Evolution.

[60]  H. Sezutsu,et al.  Significant levels of sequence divergence and gene rearrangements have occurred between the mitochondrial genomes of the wild mulberry silkmoth, Bombyx mandarina, and its close relative, the domesticated silkmoth, Bombyx mori. , 2002, Molecular biology and evolution.

[61]  Zhe‐Xi Luo,et al.  In quest for a phylogeny of Mesozoic mammals , 2002 .

[62]  J. Boore,et al.  Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. , 2002, Molecular biology and evolution.

[63]  J. Boore,et al.  Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. , 1995, Genetics.

[64]  J. Boore,et al.  The complete mitochondrial DNA sequence of the horseshoe crab Limulus polyphemus. , 2000, Molecular biology and evolution.

[65]  J. Boore,et al.  Hexapod Origins: Monophyletic or Paraphyletic? , 2003, Science.

[66]  M. Dowton,et al.  Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. , 2003, Molecular biology and evolution.

[67]  R. Gasser,et al.  The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea). , 2002, International journal for parasitology.

[68]  C. Lydeard,et al.  Complete mtDNA sequence of the North American freshwater mussel, Lampsilis ornata (Unionidae): an examination of the evolution and phylogenetic utility of mitochondrial genome organization in Bivalvia (Mollusca). , 2003, Molecular biology and evolution.

[69]  Gonzalo Giribet,et al.  Molecular Systematics and Evolution: Theory and Practice , 2002, EXS 92.

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

[71]  S. Cooper,et al.  Evolution and molecular characterization of a beta-globin gene from the Australian Echidna Tachyglossus aculeatus (Monotremata). , 1999, Molecular phylogenetics and evolution.

[72]  C. Farr,et al.  Drosophila melanogaster mitochondrial DNA: completion of the nucleotide sequence and evolutionary comparisons , 1995, Insect molecular biology.

[73]  J. Boore,et al.  Phylogenetic position of the Pentastomida and (pan)crustacean relationships , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  Kjell Nowak,et al.  A Comment on , 1975 .

[75]  Taran Grant,et al.  Data exploration in phylogenetic inference: scientific, heuristic, or neither , 2003, Cladistics : the international journal of the Willi Hennig Society.

[76]  J. Huelsenbeck,et al.  MRBAYES : Bayesian inference of phylogeny , 2001 .

[77]  Mark P. Simmons,et al.  Artifacts of Coding Amino Acids and Other Composite Characters for Phylogenetic Analysis , 2002, Cladistics : the international journal of the Willi Hennig Society.

[78]  W. Brown,et al.  Trichinella spiralis mtDNA: a nematode mitochondrial genome that encodes a putative ATP8 and normally structured tRNAS and has a gene arrangement relatable to those of coelomate metazoans. , 2001, Genetics.

[79]  R. H. Thomas,et al.  Evolution of pulmonate gastropod mitochondrial genomes: comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. , 1997, Genetics.

[80]  B. Crespi,et al.  Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers , 1994 .

[81]  P. Arruda,et al.  The mitochondrial genome of the blowfly Chrysomya chloropyga (Diptera: Calliphoridae). , 2004, Gene.

[82]  J. Boore Animal mitochondrial genomes. , 1999, Nucleic acids research.

[83]  F. Frati,et al.  The complete mitochondrial DNA sequence of the basal hexapod Tetrodontophora bielanensis: evidence for heteroplasmy and tRNA translocations. , 2001, Molecular biology and evolution.

[84]  Crotophagidae,et al.  A CLASSIFICATION OF THE LIVING BIRDS OF THE WORLD BASED ON DNA-DNA HYBRIDIZATION STUDIES , 2003 .

[85]  R. Crozier,et al.  The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. , 1993, Genetics.

[86]  G. Pritchard,et al.  Did the first insects live in water or in air , 1993 .

[87]  G. Edgecombe,et al.  Arthropod Cladistics: Combined Analysis of Histone H3 and U2 snRNA Sequences and Morphology , 2000 .

[88]  R. Gasser,et al.  The mitochondrial genome of Strongyloides stercoralis (Nematoda) - idiosyncratic gene order and evolutionary implications. , 2003, International journal for parasitology.

[89]  C. Louis,et al.  The mitochondrial genome of the Mediterranean fruit fly, Ceratitis capitata , 2000, Insect molecular biology.

[90]  T. Crease The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). , 1999, Gene.

[91]  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.

[92]  M. Miya,et al.  Complete Mitochondrial DNA Sequence of Tigriopus japonicus (Crustacea: Copepoda) , 2002, Marine Biotechnology.

[93]  L. Kruckenhauser,et al.  The complete sequence of the mitochondrial genome of Buteo buteo (Aves, Accipitridae) indicates an early split in the phylogeny of raptors. , 2001, Molecular biology and evolution.

[94]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[95]  H. Kistler,et al.  The mitochondrial genome of , 1989 .

[96]  R. Raff,et al.  Evidence for a clade of nematodes, arthropods and other moulting animals , 1997, Nature.

[97]  Francesco Nardi,et al.  Response to Comment on "Hexapod Origins: Monophyletic or Paraphyletic?" , 2003, Science.

[98]  S. Barker,et al.  The mitochondrial 12S gene is a suitable marker of populations of Sarcoptes scabiei from wombats, dogs and humans in Australia , 2002, Parasitology Research.

[99]  A. Leaché,et al.  Molecular systematics of the Eastern Fence Lizard (Sceloporus undulatus): a comparison of Parsimony, Likelihood, and Bayesian approaches. , 2002, Systematic biology.

[100]  D. Penny,et al.  The root of the mammalian tree inferred from whole mitochondrial genomes. , 2003, Molecular phylogenetics and evolution.

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

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

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

[104]  Shin-ichi Yokobori,et al.  Genetic Code Variations in Mitochondria: tRNA as a Major Determinant of Genetic Code Plasticity , 2001, Journal of Molecular Evolution.

[105]  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.

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

[107]  J. Boore,et al.  The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. , 2004, Molecular biology and evolution.

[108]  G. Giribet,et al.  The position of arthropods in the animal kingdom: a search for a reliable outgroup for internal arthropod phylogeny. , 1998, Molecular phylogenetics and evolution.

[109]  C. D’Haese Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and optimization alignment. , 2002, Proceedings. Biological sciences.

[110]  Yoshimasa Tanaka,et al.  The mitochondrial DNA of , 2000 .