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

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 who...

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Main Authors: 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
Format: Article
Language:English
Published: BMC 2017-07-01
Series:BMC Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12915-017-0399-x
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author 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_facet 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_sort Evelyn E. Schwager
collection DOAJ
description 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.
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spelling doaj.art-7f4bb216c9a44bfe9d385085f175f1b42022-12-21T18:09:47ZengBMCBMC Biology1741-70072017-07-0115112710.1186/s12915-017-0399-xThe house spider genome reveals an ancient whole-genome duplication during arachnid evolutionEvelyn E. Schwager0Prashant P. Sharma1Thomas Clarke2Daniel J. Leite3Torsten Wierschin4Matthias Pechmann5Yasuko Akiyama-Oda6Lauren Esposito7Jesper Bechsgaard8Trine Bilde9Alexandra D. Buffry10Hsu Chao11Huyen Dinh12HarshaVardhan Doddapaneni13Shannon Dugan14Cornelius Eibner15Cassandra G. Extavour16Peter Funch17Jessica Garb18Luis B. Gonzalez19Vanessa L. Gonzalez20Sam Griffiths-Jones21Yi Han22Cheryl Hayashi23Maarten Hilbrant24Daniel S. T. Hughes25Ralf Janssen26Sandra L. Lee27Ignacio Maeso28Shwetha C. Murali29Donna M. Muzny30Rodrigo Nunes da Fonseca31Christian L. B. Paese32Jiaxin Qu33Matthew Ronshaugen34Christoph Schomburg35Anna Schönauer36Angelika Stollewerk37Montserrat Torres-Oliva38Natascha Turetzek39Bram Vanthournout40John H. Werren41Carsten Wolff42Kim C. Worley43Gregor Bucher44Richard A. Gibbs45Jonathan Coddington46Hiroki Oda47Mario Stanke48Nadia A. Ayoub49Nikola-Michael Prpic50Jean-François Flot51Nico Posnien52Stephen Richards53Alistair P. McGregor54Department of Biological and Medical Sciences, Oxford Brookes UniversityDepartment of Zoology, University of Wisconsin-MadisonDepartment of Biology, Washington and Lee UniversityDepartment of Biological and Medical Sciences, Oxford Brookes UniversityErnst Moritz Arndt University Greifswald, Institute for Mathematics and Computer ScienceDepartment for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-HausJT Biohistory Research HallInstitute for Biodiversity Science and Sustainability, California Academy of SciencesDepartment of Bioscience, Aarhus UniversityDepartment of Bioscience, Aarhus UniversityDepartment of Biological and Medical Sciences, Oxford Brookes UniversityHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineDepartment of Genetics, Friedrich-Schiller-University JenaDepartment of Organismic and Evolutionary Biology, Harvard UniversityDepartment of Bioscience, Aarhus UniversityDepartment of Biological Sciences, University of Massachusetts LowellDepartment of Biological and Medical Sciences, Oxford Brookes UniversitySmithsonian National Museum of Natural History, MRC-163Faculty of Biology Medicine and Health, University of ManchesterHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineDepartment of Biology, University of CaliforniaDepartment of Biological and Medical Sciences, Oxford Brookes UniversityHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineDepartment of Earth Sciences, Palaeobiology, Uppsala UniversityHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineCentro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de OlavideHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineNucleo em Ecologia e Desenvolvimento SocioAmbiental de Macaé (NUPEM), Campus Macaé, Universidade Federal do Rio de Janeiro (UFRJ)Department of Biological and Medical Sciences, Oxford Brookes UniversityHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineFaculty of Biology Medicine and Health, University of ManchesterDepartment for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-HausDepartment of Biological and Medical Sciences, Oxford Brookes UniversitySchool of Biological and Chemical Sciences, Queen Mary University of LondonDepartment for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-HausDepartment for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-HausDepartment of Bioscience, Aarhus UniversityBiology Department, University of RochesterHumboldt-Universität of Berlin, Institut für BiologieHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineDepartment of Evolutionary Developmental Genetics, Johann-Friedrich-Blumenbach-Institute, GZMB, Georg-August-UniversityHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineSmithsonian National Museum of Natural History, MRC-163JT Biohistory Research HallErnst Moritz Arndt University Greifswald, Institute for Mathematics and Computer ScienceDepartment of Biology, Washington and Lee UniversityDepartment for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-HausUniversité libre de Bruxelles (ULB), Evolutionary Biology & EcologyDepartment for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-HausHuman Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of MedicineDepartment of Biological and Medical Sciences, Oxford Brookes UniversityAbstract 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.http://link.springer.com/article/10.1186/s12915-017-0399-xParasteatoda tepidariorumGenomeCentruroides sculpturatusGene duplicationEvolutionHox genes
spellingShingle 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
The house spider genome reveals an ancient whole-genome duplication during arachnid evolution
BMC Biology
Parasteatoda tepidariorum
Genome
Centruroides sculpturatus
Gene duplication
Evolution
Hox genes
title The house spider genome reveals an ancient whole-genome duplication during arachnid evolution
title_full The house spider genome reveals an ancient whole-genome duplication during arachnid evolution
title_fullStr The house spider genome reveals an ancient whole-genome duplication during arachnid evolution
title_full_unstemmed The house spider genome reveals an ancient whole-genome duplication during arachnid evolution
title_short The house spider genome reveals an ancient whole-genome duplication during arachnid evolution
title_sort house spider genome reveals an ancient whole genome duplication during arachnid evolution
topic Parasteatoda tepidariorum
Genome
Centruroides sculpturatus
Gene duplication
Evolution
Hox genes
url http://link.springer.com/article/10.1186/s12915-017-0399-x
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