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 Schonauer; 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-Francois 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 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. 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 Schonauer, 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-Francois Flot, Nico Posnien, Stephen Richards, Alistair P. McGregor

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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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	B M C Biology
Volume	15
Issue	1
Number of pages	27
ISSN	1741-7007
DOIs	https://doi.org/10.1186/s12915-017-0399-x
Publication status	Published - 31 Jul 2017

Keywords

Parasteatoda tepidariorum
Genome
Centruroides sculpturatus
Gene duplication
Evolution
Hox genes
MESOBUTHUS-MARTENSII REVEALS
HOX GENES
PARASTEATODA-TEPIDARIORUM
PHYLOGENETIC ANALYSES
CUPIENNIUS-SALEI
HOMEOBOX GENES
ACHAEARANEA-TEPIDARIORUM
DEVELOPMENTAL BIOLOGY
EXPRESSION PATTERNS
DOSAGE-SENSITIVITY

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Evolutionary ecology and genomics of sociality in spiders
Bilde, T. (Project manager), Bechsgaard, J. S. (Project manager) & Settepani, V. (Project manager)
Project: Research

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Schwager, E. E., Sharma, P. 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., Doddapaneni, H., Dugan, 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. B M C Biology, 15(1), Article 62. https://doi.org/10.1186/s12915-017-0399-x

@article{b56b296fe20540e991adb094b38f953c,

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 = "Parasteatoda tepidariorum, Genome, Centruroides sculpturatus, Gene duplication, Evolution, Hox genes, MESOBUTHUS-MARTENSII REVEALS, HOX GENES, PARASTEATODA-TEPIDARIORUM, PHYLOGENETIC ANALYSES, CUPIENNIUS-SALEI, HOMEOBOX GENES, ACHAEARANEA-TEPIDARIORUM, DEVELOPMENTAL BIOLOGY, EXPRESSION PATTERNS, DOSAGE-SENSITIVITY",

author = "Schwager, {Evelyn E.} and Sharma, {Prashant P.} 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 Huyen Dinh and HarshaVardhan Doddapaneni and Shannon Dugan 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 {da Fonseca}, {Rodrigo Nunes} and Paese, {Christian L. B.} and Jiaxin Qu and Matthew Ronshaugen and Christoph Schomburg and Anna Schonauer 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 Nikola-Michael Prpic and Jean-Francois Flot 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 = "B M C Biology",

issn = "1741-7007",

publisher = "BioMed Central Ltd.",

number = "1",

}

Schwager, EE, Sharma, PP, Clarke, T, Leite, DJ, Wierschin, T, Pechmann, M, Akiyama-Oda, Y, Esposito, L, Bechsgaard, J, Bilde, T, Buffry, AD, Chao, H, Dinh, H, Doddapaneni, H, Dugan, 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, da Fonseca, RN, Paese, CLB, Qu, J, Ronshaugen, M, Schomburg, C, Schonauer, 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, N-M, Flot, J-F, Posnien, N, Richards, S & McGregor, AP 2017, 'The house spider genome reveals an ancient whole-genome duplication during arachnid evolution', B M C 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 P.

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

AU - Doddapaneni, HarshaVardhan

AU - Dugan, 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 - da Fonseca, Rodrigo Nunes

AU - Paese, Christian L. B.

AU - Qu, Jiaxin

AU - Ronshaugen, Matthew

AU - Schomburg, Christoph

AU - Schonauer, 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-Francois

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 - Parasteatoda tepidariorum

KW - Genome

KW - Centruroides sculpturatus

KW - Gene duplication

KW - Evolution

KW - Hox genes

KW - MESOBUTHUS-MARTENSII REVEALS

KW - HOX GENES

KW - PARASTEATODA-TEPIDARIORUM

KW - PHYLOGENETIC ANALYSES

KW - CUPIENNIUS-SALEI

KW - HOMEOBOX GENES

KW - ACHAEARANEA-TEPIDARIORUM

KW - DEVELOPMENTAL BIOLOGY

KW - EXPRESSION PATTERNS

KW - DOSAGE-SENSITIVITY

U2 - 10.1186/s12915-017-0399-x

DO - 10.1186/s12915-017-0399-x

M3 - Journal article

C2 - 28756775

SN - 1741-7007

VL - 15

JO - B M C Biology

JF - B M C Biology

IS - 1

M1 - 62

ER -

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

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Evolutionary ecology and genomics of sociality in spiders

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