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Phylogenomic Interrogation of Arachnida Reveals Systemic Conflicts in Phylogenetic Signal

Sharma, Prashant P., Kaluziak, Stefan T., Pérez-Porro, Alicia R., González, Vanessa L., Hormiga, Gustavo, Wheeler, Ward C., Giribet, Gonzalo·2014·Molecular Biology and Evolution
DOI 10.1093/molbev/msu235
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Abstract

Chelicerata represents one of the oldest groups of arthropods, with a fossil record extending to the Cambrian, and is sister group to the remaining extant arthropods, the mandibulates. Attempts to resolve the internal phylogeny of chelicerates have achieved little consensus, due to marked discord in both morphological and molecular hypotheses of chelicerate phylogeny. The monophyly of Arachnida, the terrestrial chelicerates, is generally accepted, but has garnered little support from molecular data, which have been limited either in breadth of taxonomic sampling or in depth of sequencing. To address the internal phylogeny of this group, we employed a phylogenomic approach, generating transcriptomic data for 17 species in combination with existing data, including two complete genomes. We analyzed multiple data sets containing up to 1,235,912 sites across 3,644 loci, using alternative approaches to optimization of matrix composition. Here, we show that phylogenetic signal for the monophyly of Arachnida is restricted to the 500 slowest-evolving genes in the data set. Accelerated evolutionary rates in Acariformes, Pseudoscorpiones, and Parasitiformes potentially engender long-branch attraction artifacts, yielding nonmonophyly of Arachnida with increasing support upon incrementing the number of concatenated genes. Mutually exclusive hypotheses are supported by locus groups of variable evolutionary rate, revealing significant conflicts in phylogenetic signal. Analyses of gene-tree discordance indicate marked incongruence in relationships among chelicerate orders, whereas derived relationships are demonstrably robust. Consistently recovered and supported relationships include the monophyly of Chelicerata, Euchelicerata, Tetrapulmonata, and all orders represented by multiple terminals. Relationships supported by subsets of slow-evolving genes include Ricinulei + Solifugae; a clade comprised of Ricinulei, Opiliones, and Solifugae; and a clade comprised of Tetrapulmonata, Scorpiones, and Pseudoscorpiones. We demonstrate that outgroup selection without regard for branch length distribution exacerbates long-branch attraction artifacts and does not mitigate gene-tree discordance, regardless of high gene representation for outgroups that are model organisms. Arachnopulmonata (new name) is proposed for the clade comprising Scorpiones + Tetrapulmonata (previously named Pulmonata).

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Research works printed but not linked: 94

  1. Altenhoff, 2013, Inferring hierarchical orthologous groups from orthologous gene pairs, PLoS One, 8, e53786, 10.1371/journal.pone.0053786 · DOI
  2. Arabi, 2012, Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): detecting new mitogenomic rearrangements, J Mol Evol., 74, 81, 10.1007/s00239-012-9490-7 · DOI
  3. Barnett, 2013, The expression of limb gap genes in the mite Archegozetes longisetosus reveals differential patterning mechanisms in chelicerates, Evol Dev., 15, 280, 10.1111/ede.12038 · DOI
  4. Berger, 2011, Performance, accuracy, and Web server for evolutionary placement of short sequence reads under maximum likelihood, Syst Biol., 60, 291, 10.1093/sysbio/syr010 · DOI · Paper page
  5. Betancur-R, 2014, Conserved genes, sampling error, and phylogenomic inference, Syst Biol., 63, 257, 10.1093/sysbio/syt073 · DOI
  6. Brewer, 2013, Ordinal-level phylogenomics of the arthropod class Diplopoda (millipedes) based on an analysis of 221 nuclear protein-coding loci generated using next-generation sequence analyses, PLoS One, 8, e79935, 10.1371/journal.pone.0079935 · DOI
  7. Briggs, 2012, Silurian horseshoe crab illuminates the evolution of arthropod limbs, Proc Natl Acad Sci U S A., 109, 15702, 10.1073/pnas.1205875109 · DOI
  8. Campbell, 2011, MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda, Proc Natl Acad Sci U S A., 108, 15920, 10.1073/pnas.1105499108 · DOI
  9. Cao, 2013, The genome of Mesobuthus martensii reveals a unique adaptation model of arthropods, Nat Commun., 4, 2602, 10.1038/ncomms3602 · DOI
  10. Castresana, 2000, Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis, Mol Biol Evol., 17, 540, 10.1093/oxfordjournals.molbev.a026334 · DOI · Paper page
  11. Clouse, 2013, Elongation factor-1α, a putative single-copy nuclear gene, has divergent sets of paralogs in an arachnid, Mol Phylogenet Evol., 68, 471, 10.1016/j.ympev.2013.04.025 · DOI
  12. Coddington, 2004, Arachnida, 296, 10.1093/oso/9780195172348.003.0019 · DOI
  13. Dell’Ampio, 2014, Decisive data sets in phylogenomics: lessons from studies on the phylogenetic relationships of primarily wingless insects, Mol Biol Evol., 31, 239, 10.1093/molbev/mst196 · DOI
  14. Dunlop, 2010, Geological history and phylogeny of Chelicerata, Arthropod Struct Dev., 39, 124, 10.1016/j.asd.2010.01.003 · DOI
  15. Dunlop, 2007, Reinterpreting the morphology of the Jurassic scorpion Liassoscorpionides, Arthropod Struct Dev., 36, 245, 10.1016/j.asd.2006.09.003 · DOI
  16. Dunlop, 2012, The sejugal furrow in camel spiders and acariform mites, Arachnol Mitt., 43, 8
  17. Dunlop, 1999, Fossil evidence, terrestrialization, and arachnid phylogeny, J Arachnol., 27, 86
  18. Edgar, 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 32, 1792, 10.1093/nar/gkh340 · DOI · Paper page
  19. Emerson, 1998, Theories, patterns, and reality: game plan for arthropod phylogeny, 67, 10.1007/978-94-011-4904-4_7 · DOI
  20. Ewen-Campen, 2011, The maternal and early embryonic transcriptome of the milkweed bug Oncopeltus fasciatus, BMC Genomics, 12, 61, 10.1186/1471-2164-12-61 · DOI
  21. Felsenstein, 1978, Cases in which parsimony or compatibility methods will be positively misleading, Syst Biol., 27, 401, 10.1093/sysbio/27.4.401 · DOI
  22. Fernández, 2014, Evaluating topological conflict in centipede phylogeny using transcriptomic data sets, Mol Biol Evol., 31, 1500, 10.1093/molbev/msu108 · DOI
  23. Firstman, 1973, The relationship of the chelicerate arterial system to the evolution of the endosternite, J Arachnol., 1, 1
  24. Friedrich, 1995, Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods, Nature, 376, 165, 10.1038/376165a0 · DOI · Paper page
  25. Giribet, 1996, First molecular evidence for the existence of a Tardigrada + Arthropoda clade, Mol Biol Evol., 13, 76, 10.1093/oxfordjournals.molbev.a025573 · DOI
  26. Giribet, 2001, Arthropod phylogeny based on eight molecular loci and morphology, Nature, 413, 157, 10.1038/35093097 · DOI · Paper page
  27. Giribet, 2002, Phylogeny and systematic position of Opiliones: a combined analysis of chelicerate relationships using morphological and molecular data, Cladistics, 18, 5
  28. Giribet, 2014, The first phylogenetic analysis of Palpigradi (Arachnida)—the most enigmatic arthropod order, Invertebr Syst., 28, 10.1071/IS13057 · DOI
  29. Giribet, 1998, The position of arthropods in the animal kingdom: a search of a reliable outgroup for internal arthropod phylogeny, Mol Phylogenet Evol., 9, 481, 10.1006/mpev.1998.0494 · DOI
  30. Giribet, 2010, A multilocus approach to harvestmen (Arachnida: Opiliones) phylogeny with emphasis on biogeography and the systematics of Laniatores, Cladistics, 26, 408, 10.1111/j.1096-0031.2009.00296.x · DOI
  31. Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat Biotechnol., 29, 644, 10.1038/nbt.1883 · DOI · Paper page
  32. Grbic, 2011, The genome of Tetranychus urticae reveals herbivorous pest adaptations, Nature, 479, 487, 10.1038/nature10640 · DOI · Paper page
  33. Grünewald, 2013, SuperQ: computing supernetworks from quartets, IEEE/ACM Trans Comput Biol Bioinform., 10, 151, 10.1109/TCBB.2013.8 · DOI
  34. Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis, Nat Protoc., 8, 1494, 10.1038/nprot.2013.084 · DOI · Paper page
  35. Hedin, 2010, The phylogenetic utility of the nuclear protein-coding gene EF-1α for resolving recent divergences in Opiliones, emphasizing intron evolution, J Arachnol., 38, 9, 10.1636/HA09-49.1 · DOI
  36. Hedin, 2012, Phylogenomic resolution of Paleozoic divergences in harvestmen (Arachnida, Opiliones) via analysis of next-generation transcriptome data, PLoS One, 7, e42888, 10.1371/journal.pone.0042888 · DOI
  37. Huelsenbeck, 1997, Is the Felsenstein zone a fly trap?, Syst Biol., 46, 69, 10.1093/sysbio/46.1.69 · DOI
  38. Hughes, 2002, Hox genes and the evolution of the arthropod body plan, Evol Dev., 4, 459, 10.1046/j.1525-142X.2002.02034.x · DOI · Paper page
  39. Jeram, 1998, Phylogeny, classifications and evolution of Silurian and Devonian scorpions, 17
  40. Kamenz, 2008, Microanatomy of Early Devonian book lungs, Biol Lett., 4, 212, 10.1098/rsbl.2007.0597 · DOI
  41. Khila, 2007, Gene silencing in the spider mite Tetranychus urticae: dsRNA and siRNA parental silencing of the Distal-less gene, Dev Genes Evol., 217, 241, 10.1007/s00427-007-0132-9 · DOI
  42. Koenemann, 2010, Arthropod phylogeny revisited, with a focus on crustacean relationships, Arthropod Struct Dev., 39, 88, 10.1016/j.asd.2009.10.003 · DOI
  43. Kraus, 1998, Phylogenetic relationships between higher taxa of tracheate arthropods, 295, 10.1007/978-94-011-4904-4_22 · DOI
  44. Kubatko, 2007, Inconsistency of phylogenetic estimates from concatenated data under coalescence, Syst Biol., 56, 17, 10.1080/10635150601146041 · DOI · Paper page
  45. Lamsdell, 2013, Revised systematics of Palaeozoic ‘horseshoe crabs’ and the myth of monophyletic Xiphosura, Zool J Linn Soc., 167, 1, 10.1111/j.1096-3642.2012.00874.x · DOI
  46. Lartillot, 2004, A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process, Mol Biol Evol., 21, 1095, 10.1093/molbev/msh112 · DOI · Paper page
  47. Lartillot, 2008, Improvement of molecular phylogenetic inference and the phylogeny of Bilateria, Philos Trans R Soc Lond B Biol Sci., 363, 1463, 10.1098/rstb.2007.2236 · DOI
  48. Le, 2012, Modeling protein evolution with several amino acid replacement matrices depending on site rates, Mol Biol Evol., 29, 2921, 10.1093/molbev/mss112 · DOI · Paper page
  49. Legg, 2013, Arthropod fossil data increase congruence of morphological and molecular phylogenies, Nat Commun., 4, 2485, 10.1038/ncomms3485 · DOI
  50. Mallatt, 2004, Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin, Mol. Phylogenet. Evol., 31, 178, 10.1016/j.ympev.2003.07.013 · DOI · Paper page
  51. Masta, 2009, Arachnid relationships based on mitochondrial genomes: asymmetric nucleotide and amino acid bias affects phylogenetic analyses, Mol Phylogenet Evol., 50, 117, 10.1016/j.ympev.2008.10.010 · DOI
  52. Masta, 2010, Rare genomic changes and mitochondrial sequences provide independent support for congruent relationships among the sea spiders (Arthropoda, Pycnogonida), Mol Phylogenet Evol., 57, 59, 10.1016/j.ympev.2010.06.020 · DOI
  53. Meusemann, 2010, A phylogenomic approach to resolve the arthropod tree of life, Mol Biol Evol., 27, 2451, 10.1093/molbev/msq130 · DOI · Paper page
  54. Narechania, 2012, 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, Genome Biol Evol., 4, 30, 10.1093/gbe/evr121 · DOI
  55. Nieselt-Struwe, 2001, Quartet-mapping, a generalization of the likelihood-mapping procedure, Mol Biol Evol., 18, 1204, 10.1093/oxfordjournals.molbev.a003907 · DOI
  56. Obst, 2012, Molecular phylogeny of extant horseshoe crabs (Xiphosura, Limulidae) indicates Paleogene diversification of Asian species, Mol Phylogenet Evol., 62, 21, 10.1016/j.ympev.2011.08.025 · DOI
  57. Pepato, 2010, Phylogenetic position of the acariform mites: sensitivity to homology assessment under total evidence, BMC Evol Biol., 10, 235, 10.1186/1471-2148-10-235 · DOI
  58. Philippe, 2009, Phylogenomics revives traditional views on deep animal relationships, Curr Biol., 19, 706, 10.1016/j.cub.2009.02.052 · DOI · Paper page
  59. Philippe, 2005, Heterotachy and long-branch attraction in phylogenetics, BMC Evol Biol., 5, 50, 10.1186/1471-2148-5-50 · DOI · Paper page
  60. Prpic, 2004, Expression patterns of leg genes in the mouthparts of the spider Cupiennius salei (Chelicerata: Arachnida), Dev Genes Evol., 214, 296, 10.1007/s00427-004-0393-5 · DOI
  61. Regier, 2010, Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences, Nature, 463, 1079, 10.1038/nature08742 · DOI · Paper page
  62. Rehm, 2014, Phylogenetic position of Myriapoda revealed by 454 transcriptomic sequencing, Mol Phylogenet Evol., 77, 25, 10.1016/j.ympev.2014.04.007 · DOI
  63. Riesgo, 2012, Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa, Front Zool., 9, 33, 10.1186/1742-9994-9-33 · DOI
  64. Roeding, 2009, A 454 sequencing approach for large scale phylogenomic analysis of the common emperor scorpion (Pandinus imperator), Mol Phylogenet Evol., 53, 826, 10.1016/j.ympev.2009.08.014 · DOI
  65. Rokas, 2003, Conflicting phylogenetic signals at the base of the metazoan tree, Evol Dev., 5, 346, 10.1046/j.1525-142X.2003.03042.x · DOI
  66. Rota-Stabelli, 2011, A congruent solution to arthropod phylogeny: phylogenomics, microRNAs and morphology support monophyletic Mandibulata, Proc R Soc Lond B Biol Sci., 278, 298, 10.1098/rspb.2010.0590 · DOI · Paper page
  67. Rota-Stabelli, 2008, A multi criterion approach for the selection of optimal outgroups in phylogeny: recovering some support for Mandibulata over Myriochelata using mitogenomics, Mol Phylogenet Evol., 48, 103, 10.1016/j.ympev.2008.03.033 · DOI
  68. Scholtz, 2006, The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): evidence for homology and a single terrestrialization event of a common arachnid ancestor, Zoology, 109, 2, 10.1016/j.zool.2005.06.003 · DOI
  69. Schoppmeier, 2001, Double-stranded RNA interference in the spider Cupiennius salei: the role of Distal-less is evolutionarily conserved in arthropod appendage formation, Dev Genes Evol., 211, 76, 10.1007/s004270000121 · DOI
  70. Schram, 1991, Arthropod pattern theory: a new approach to arthropod phylogeny, Mem Queensl Mus., 31, 1
  71. Sharma, 2011, The evolutionary and biogeographic history of the armoured harvestmen—Laniatores phylogeny based on ten molecular markers, with the description of two new families of Opiliones (Arachnida), Invertebr Syst., 25, 106, 10.1071/IS11002 · DOI
  72. Sharma, 2012, Evolution of the chelicera: a dachshund domain is retained in the deutocerebral appendage of Opiliones (Arthropoda, Chelicerata), Evol Dev., 14, 522, 10.1111/ede.12005 · DOI
  73. Sharma, 2012, Hox gene expression in the harvestman Phalangium opilio reveals divergent patterning of the chelicerate opisthosoma, Evol Dev., 14, 450, 10.1111/j.1525-142X.2012.00565.x · DOI
  74. Sharma, 2014, Hox gene duplications correlate with posterior heteronomy in scorpions, Proc R Soc Lond B Biol Sci., 281, 20140661, 10.1098/rspb.2014.0661 · DOI
  75. Sharma, 2013, Distal-less and dachshund pattern both plesiomorphic and apomorphic structures in chelicerates: RNA interference in the harvestman Phalangium opilio (Opiliones), Evol Dev., 15, 228, 10.1111/ede.12029 · DOI
  76. Shultz, 1990, Evolutionary morphology and phylogeny of Arachnida, Cladistics, 6, 1, 10.1111/j.1096-0031.1990.tb00523.x · DOI
  77. Shultz, 1998, Phylogeny of Opiliones (Arachnida): an assessment of the “Cyphopalpatores” concept, J Arachnol., 26, 257
  78. Shultz, 2007, A phylogenetic analysis of the arachnid orders based on morphological characters, Zool J Linn Soc., 150, 221, 10.1111/j.1096-3642.2007.00284.x · DOI · Paper page
  79. Simon, 2012, Insect phylogenomics: exploring the source of incongruence using new transcriptomic data, Genome Biol Evol., 4, 1295, 10.1093/gbe/evs104 · DOI
  80. Smith, 2008, Phyutility: a phyloinformatics tool for trees, alignments and molecular data, Bioinformatics, 24, 715, 10.1093/bioinformatics/btm619 · DOI · Paper page
  81. Snodgrass, 1938, Evolution of the Annelida, Onychophora and Arthropoda, Smithson. Misc. Collect., 97, 1
  82. Stamatakis, 2008, A rapid bootstrap algorithm for the RAxML Web servers, Syst Biol., 57, 758, 10.1080/10635150802429642 · DOI · Paper page
  83. Turbeville, 1991, The phylogenetic status of arthropods, as inferred from 18S rRNA sequences, Mol Biol Evol., 8, 669
  84. Van der Hammen, 1989, An introduction to comparative arachnology
  85. von Reumont, 2012, Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda, Mol Biol Evol., 29, 1031, 10.1093/molbev/msr270 · DOI
  86. Weygoldt, 1979, Untersuchungen zur Morphologie, Taxonomie und Phylogenie der Chelicerata, Z Zool Syst Evol., 17, 85, 10.1111/j.1439-0469.1979.tb00694.x · DOI
  87. Wheeler, 1998, Sampling, groundplans, total evidence and the systematics of arthropods, 87, 10.1007/978-94-011-4904-4_8 · DOI
  88. Wheeler, 1993, Arthropod phylogeny: a combined approach, Cladistics, 14, 173, 10.1111/j.1096-0031.1998.tb00331.x · DOI · Paper page
  89. Wheeler, 1998, The phylogeny of the extant chelicerate orders, Cladistics, 14, 173, 10.1111/j.1096-0031.1998.tb00331.x · DOI · Paper page
  90. Wiens, 2006, Missing data and the design of phylogenetic analyses, J Biomed Inform., 39, 34, 10.1016/j.jbi.2005.04.001 · DOI · Paper page
  91. Wilcox, 2004, Convergence among cave catfishes: long-branch attraction and a Bayesian relative rates test, Mol Phylogenet Evol., 31, 1101, 10.1016/j.ympev.2003.11.006 · DOI
  92. Wirkner, 2013, The arthropod circulatory system, 343, 10.1007/978-3-662-45798-6_14 · DOI
  93. Zeng, 2011, De novo assembly and characterization of a maternal and developmental transcriptome for the emerging model crustacean Parhyale hawaiensis, BMC Genomics, 12, 581, 10.1186/1471-2164-12-581 · DOI
  94. Zrzavý, 1998, Arthropod phylogeny: taxonomic congruence, total evidence and conditional combination approaches to morphological and molecular data sets, 97, 10.1007/978-94-011-4904-4_9 · DOI

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Metadata

Authors
Sharma, P. P., Kaluziak, S. T., Pérez-Porro, A. R., González, V. L., Hormiga, G., Wheeler, W. C., & Giribet, G.
Venue
Molecular Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2014-08-08
Volume
31
Issue
11
Pages
2963-2984
ISSN
  • 0737-4038 (ISSN-L)
  • 1537-1719
DOI
10.1093/molbev/msu235
OpenAlex
W2111710925
Cited by
326
References
15
FWCI
11.56
Type
journal article
Language
en
Open access
closed

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