The house spider genome reveals an ancient whole-genome duplication during arachnid evolution.

Evelyn E Schwager, Prashant P Sharma, Thomas Clarke, Daniel J Leite, Torsten Wierschin, Matthias Pechmann, Yasuko Akiyama-Oda, Lauren Esposito, Jesper Bechsgaard, Trine Bilde, Alexandra D Buffry, Hsu Chao, Huyen Dinh, HarshaVardhan Doddapaneni, Shannon Dugan, Cornelius Eibner, Cassandra G Extavour, Peter Funch, Jessica Garb, Luis B Gonzalez, Vanessa L Gonzalez, Sam Griffiths-Jones, Yi Han, Cheryl Hayashi, Maarten Hilbrant, Daniel S T Hughes, Ralf Janssen, Sandra L Lee, Ignacio Maeso, Shwetha C Murali, Donna M Muzny, Rodrigo Nunes da Fonseca, Christian L B Paese, Jiaxin Qu, Matthew Ronshaugen, Christoph Schomburg, Anna Schönauer, Angelika Stollewerk, Montserrat Torres-Oliva, Natascha Turetzek, Bram Vanthournout, John H Werren, Carsten Wolff, Kim C Worley, Gregor Bucher, Richard A Gibbs, Jonathan Coddington, Hiroki Oda, Mario Stanke, Nadia A Ayoub, Nikola-Michael Prpic, Jean-François Flot, Nico Posnien, Stephen Richards, Alistair P McGregor
Author Information
  1. Evelyn E Schwager: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
  2. Prashant P Sharma: Department of Zoology, University of Wisconsin-Madison, 430 Lincoln Drive, Madison, WI, 53706, USA.
  3. Thomas Clarke: Department of Biology, Washington and Lee University, 204 West Washington Street, Lexington, VA, 24450, USA.
  4. Daniel J Leite: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
  5. Torsten Wierschin: Ernst Moritz Arndt University Greifswald, Institute for Mathematics and Computer Science, Walther-Rathenau-Str. 47, 17487, Greifswald, Germany.
  6. Matthias Pechmann: Department for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Goettingen, Germany.
  7. Yasuko Akiyama-Oda: JT Biohistory Research Hall, 1-1 Murasaki-cho, Takatsuki, Osaka, 569-1125, Japan.
  8. Lauren Esposito: Institute for Biodiversity Science and Sustainability, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA, 94118, USA.
  9. Jesper Bechsgaard: Department of Bioscience, Aarhus University, Ny Munkegade 116, building 1540, 8000, Aarhus C, Denmark.
  10. Trine Bilde: Department of Bioscience, Aarhus University, Ny Munkegade 116, building 1540, 8000, Aarhus C, Denmark.
  11. Alexandra D Buffry: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
  12. Hsu Chao: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  13. Huyen Dinh: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  14. HarshaVardhan Doddapaneni: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  15. Shannon Dugan: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  16. Cornelius Eibner: Department of Genetics, Friedrich-Schiller-University Jena, Philosophenweg 12, 07743, Jena, Germany.
  17. Cassandra G Extavour: Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA, 02138, USA.
  18. Peter Funch: Department of Bioscience, Aarhus University, Ny Munkegade 116, building 1540, 8000, Aarhus C, Denmark.
  19. Jessica Garb: Department of Biological Sciences, University of Massachusetts Lowell, 198 Riverside Street, Lowell, MA, 01854, USA.
  20. Luis B Gonzalez: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
  21. Vanessa L Gonzalez: Smithsonian National Museum of Natural History, MRC-163, P.O. Box 37012, Washington, DC, 20013-7012, USA.
  22. Sam Griffiths-Jones: Faculty of Biology Medicine and Health, University of Manchester, D.1416 Michael Smith Building, Oxford Road, Manchester, M13 9PT, UK.
  23. Yi Han: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  24. Cheryl Hayashi: Department of Biology, University of California, Riverside, Riverside, CA, 92521, USA.
  25. Maarten Hilbrant: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
  26. Daniel S T Hughes: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  27. Ralf Janssen: Department of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, 75236, Uppsala, Sweden.
  28. Sandra L Lee: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  29. Ignacio Maeso: Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide, Sevilla, Spain.
  30. Shwetha C Murali: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  31. Donna M Muzny: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  32. Rodrigo Nunes da Fonseca: Nucleo em Ecologia e Desenvolvimento SocioAmbiental de Macaé (NUPEM), Campus Macaé, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, 27941-222, Brazil.
  33. Christian L B Paese: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
  34. Jiaxin Qu: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  35. Matthew Ronshaugen: Faculty of Biology Medicine and Health, University of Manchester, D.1416 Michael Smith Building, Oxford Road, Manchester, M13 9PT, UK.
  36. Christoph Schomburg: Department for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Goettingen, Germany.
  37. Anna Schönauer: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
  38. Angelika Stollewerk: School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, E1 4NS, London, UK.
  39. Montserrat Torres-Oliva: Department for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Goettingen, Germany.
  40. Natascha Turetzek: Department for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Goettingen, Germany.
  41. Bram Vanthournout: Department of Bioscience, Aarhus University, Ny Munkegade 116, building 1540, 8000, Aarhus C, Denmark.
  42. John H Werren: Biology Department, University of Rochester, Rochester, NY, 14627, USA.
  43. Carsten Wolff: Humboldt-Universität of Berlin, Institut für Biologie, Philippstr.13, 10115, Berlin, Germany.
  44. Kim C Worley: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
  45. Gregor Bucher: Department of Evolutionary Developmental Genetics, Johann-Friedrich-Blumenbach-Institute, GZMB, Georg-August-University, Göttingen Campus, Justus von Liebig Weg 11, 37077, Göttingen, Germany. gbucher1@gwdg.de.
  46. Richard A Gibbs: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. agibbs@bcm.edu.
  47. Jonathan Coddington: Smithsonian National Museum of Natural History, MRC-163, P.O. Box 37012, Washington, DC, 20013-7012, USA. coddington@si.edu.
  48. Hiroki Oda: JT Biohistory Research Hall, 1-1 Murasaki-cho, Takatsuki, Osaka, 569-1125, Japan. hoda@brh.co.jp.
  49. Mario Stanke: Ernst Moritz Arndt University Greifswald, Institute for Mathematics and Computer Science, Walther-Rathenau-Str. 47, 17487, Greifswald, Germany. mario.stanke@uni-greifswald.de.
  50. Nadia A Ayoub: Department of Biology, Washington and Lee University, 204 West Washington Street, Lexington, VA, 24450, USA. ayoubn@wlu.edu.
  51. Nikola-Michael Prpic: Department for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Goettingen, Germany. nprpic@uni-goettingen.de.
  52. Jean-François Flot: Université libre de Bruxelles (ULB), Evolutionary Biology & Ecology, C.P. 160/12, Avenue F.D. Roosevelt 50, 1050, Brussels, Belgium. jflot@ulb.ac.be.
  53. Nico Posnien: Department for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Goettingen, Germany. nico.posnien@biologie.uni-goettingen.de.
  54. Stephen Richards: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. stephenr@bcm.edu.
  55. Alistair P McGregor: Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK. amcgregor@brookes.ac.uk.

Abstract

BACKGROUND: The duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum.
RESULTS: We found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication.
CONCLUSIONS: Our results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes.

Keywords

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Grants

  1. U54 HG003273/NHGRI NIH HHS

MeSH Term

Animals
Evolution, Molecular
Female
Gene Duplication
Genome
Male
Spiders
Synteny

Word Cloud

Created with Highcharts 10.0.0duplicationgenesgenometepidariorumincludingWGDcommonspiderHoxsuggestsancientspidersevolutionarytwohorseshoecrabssequencedhouseParasteatodafoundacrossPCentruroidessculpturatuseventancestorscorpionsBACKGROUND:canoccurvariousmechanismsthoughtmakemajorcontributiondiversificationorganismsincreasingevidencelarge-scalecheliceratelineagesroundswholeinvestigateanalyzedRESULTS:pervasivecodingnon-codingclustersAnalysissyntenyconservationComparisongenomescheliceratesnewlybarkscorpionoccurredprobablyindependentWGDsFurthermorecharacterizationsequenceexpressionparalogsmanysubjectneo-functionalizationand/orsub-functionalizationsinceCONCLUSIONS:resultsreveallikelydescendantspolyploidlived450MYAGivenextensivemorphologicaldiversityecologicaladaptationsamonganimalsrivalingvertebratesstudyArachnopulmonataprovidesnewcomparativeplatformexploredivergentoutcomespolyploidizationeventseukaryotesrevealswhole-genomearachnidevolutionEvolutionGeneGenome

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