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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BMC
2017-07-01
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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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language | English |
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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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