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

Evelyn E. Schwager; Prashant 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 H Dinh; Harsha Vardhan Doddapaneni; Shannon Dugan-Rocha; 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

doi:10.1186/s12915-017-0399-x

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

Evelyn E. Schwager, Prashant 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 H Dinh, Harsha Vardhan Doddapaneni, Shannon Dugan-Rocha, Cornelius Eibner, Cassandra G Extavour, Peter Funch, Jessica Garb, Luis B. GonzalezVanessa 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

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Article number	62
Journal	BMC Biology
Volume	15
Issue number	1
DOIs	https://doi.org/10.1186/s12915-017-0399-x
Publication status	Published - 31 Jul 2017

Keywords

Centruroides sculpturatus
Evolution
Gene duplication
Genome
Hox genes
Parasteatoda tepidariorum

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Schwager, E. E., Sharma, P., Clarke, T., Leite, D. J., Wierschin, T., Pechmann, M., Akiyama-Oda, Y., Esposito, L., Bechsgaard, J., Bilde, T., Buffry, A. D., Chao, H., Dinh, H. H., Doddapaneni, H. V., Dugan-Rocha, S., Eibner, C., Extavour, C. G., Funch, P., Garb, J., ... McGregor, A. P. (2017). The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biology, 15(1), Article 62. https://doi.org/10.1186/s12915-017-0399-x

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title = "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 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 = "Centruroides sculpturatus, Evolution, Gene duplication, Genome, Hox genes, Parasteatoda tepidariorum",

author = "Schwager, {Evelyn E.} and Prashant Sharma and Thomas Clarke and Leite, {Daniel J} and Torsten Wierschin and Matthias Pechmann and Yasuko Akiyama-Oda and Lauren Esposito and Jesper Bechsgaard and Trine Bilde and Buffry, {Alexandra D.} and Hsu Chao and Dinh, {Huyen H} and Doddapaneni, {Harsha Vardhan} and Shannon Dugan-Rocha and Cornelius Eibner and Extavour, {Cassandra G} and Peter Funch and Jessica Garb and Gonzalez, {Luis B.} and Gonzalez, {Vanessa L.} and Sam Griffiths-Jones and Yi Han and Cheryl Hayashi and Maarten Hilbrant and Hughes, {Daniel S T} and Ralf Janssen and Lee, {Sandra L} and Ignacio Maeso and Murali, {Shwetha C.} and Muzny, {Donna M} and {Nunes da Fonseca}, Rodrigo and Paese, {Christian L.B.} and Jiaxin Qu and Matthew Ronshaugen and Christoph Schomburg and Anna Sch{\"o}nauer and Angelika Stollewerk and Montserrat Torres-Oliva and Natascha Turetzek and Bram Vanthournout and Werren, {John H.} and Carsten Wolff and Worley, {Kim C} and Gregor Bucher and Gibbs, {Richard A} and Jonathan Coddington and Hiroki Oda and Mario Stanke and Ayoub, {Nadia A.} and Prpic, {Nikola Michael} and Flot, {Jean Fran{\c c}ois} and Nico Posnien and Stephen Richards and McGregor, {Alistair P.}",

year = "2017",

month = jul,

day = "31",

doi = "10.1186/s12915-017-0399-x",

language = "English",

volume = "15",

journal = "BMC Biology",

issn = "1741-7007",

publisher = "Springer Nature",

number = "1",

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Schwager, EE, Sharma, P, Clarke, T, Leite, DJ, Wierschin, T, Pechmann, M, Akiyama-Oda, Y, Esposito, L, Bechsgaard, J, Bilde, T, Buffry, AD, Chao, H, Dinh, HH, Doddapaneni, HV, Dugan-Rocha, S, Eibner, C, Extavour, CG, Funch, P, Garb, J, Gonzalez, LB, Gonzalez, VL, Griffiths-Jones, S, Han, Y, Hayashi, C, Hilbrant, M, Hughes, DST, Janssen, R, Lee, SL, Maeso, I, Murali, SC, Muzny, DM, Nunes da Fonseca, R, Paese, CLB, Qu, J, Ronshaugen, M, Schomburg, C, Schönauer, A, Stollewerk, A, Torres-Oliva, M, Turetzek, N, Vanthournout, B, Werren, JH, Wolff, C, Worley, KC, Bucher, G, Gibbs, RA, Coddington, J, Oda, H, Stanke, M, Ayoub, NA, Prpic, NM, Flot, JF, Posnien, N, Richards, S & McGregor, AP 2017, 'The house spider genome reveals an ancient whole-genome duplication during arachnid evolution', BMC Biology, vol. 15, no. 1, 62. https://doi.org/10.1186/s12915-017-0399-x

TY - JOUR

T1 - The house spider genome reveals an ancient whole-genome duplication during arachnid evolution

AU - Schwager, Evelyn E.

AU - Sharma, Prashant

AU - Clarke, Thomas

AU - Leite, Daniel J

AU - Wierschin, Torsten

AU - Pechmann, Matthias

AU - Akiyama-Oda, Yasuko

AU - Esposito, Lauren

AU - Bechsgaard, Jesper

AU - Bilde, Trine

AU - Buffry, Alexandra D.

AU - Chao, Hsu

AU - Dinh, Huyen H

AU - Doddapaneni, Harsha Vardhan

AU - Dugan-Rocha, Shannon

AU - Eibner, Cornelius

AU - Extavour, Cassandra G

AU - Funch, Peter

AU - Garb, Jessica

AU - Gonzalez, Luis B.

AU - Gonzalez, Vanessa L.

AU - Griffiths-Jones, Sam

AU - Han, Yi

AU - Hayashi, Cheryl

AU - Hilbrant, Maarten

AU - Hughes, Daniel S T

AU - Janssen, Ralf

AU - Lee, Sandra L

AU - Maeso, Ignacio

AU - Murali, Shwetha C.

AU - Muzny, Donna M

AU - Nunes da Fonseca, Rodrigo

AU - Paese, Christian L.B.

AU - Qu, Jiaxin

AU - Ronshaugen, Matthew

AU - Schomburg, Christoph

AU - Schönauer, Anna

AU - Stollewerk, Angelika

AU - Torres-Oliva, Montserrat

AU - Turetzek, Natascha

AU - Vanthournout, Bram

AU - Werren, John H.

AU - Wolff, Carsten

AU - Worley, Kim C

AU - Bucher, Gregor

AU - Gibbs, Richard A

AU - Coddington, Jonathan

AU - Oda, Hiroki

AU - Stanke, Mario

AU - Ayoub, Nadia A.

AU - Prpic, Nikola Michael

AU - Flot, Jean François

AU - Posnien, Nico

AU - Richards, Stephen

AU - McGregor, Alistair P.

PY - 2017/7/31

Y1 - 2017/7/31

N2 - 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.

AB - 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.

KW - Centruroides sculpturatus

KW - Evolution

KW - Gene duplication

KW - Genome

KW - Hox genes

KW - Parasteatoda tepidariorum

UR - http://www.scopus.com/inward/record.url?scp=85026443070&partnerID=8YFLogxK

U2 - 10.1186/s12915-017-0399-x

DO - 10.1186/s12915-017-0399-x

M3 - Article

AN - SCOPUS:85026443070

SN - 1741-7007

VL - 15

JO - BMC Biology

JF - BMC Biology

IS - 1

M1 - 62

ER -

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

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Keywords

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