Gene content evolution in the arthropods

Gregg W.C. Thomas; Elias Dohmen; Daniel S.T. Hughes; Shwetha C. Murali; Monica Poelchau; Karl Glastad; Clare A. Anstead; Nadia A. Ayoub; Phillip Batterham; Michelle Bellair; Greta J. Binford; Hsu Chao; Yolanda H. Chen; Christopher Childers; Huyen Dinh; Harsha Vardhan Doddapaneni; Jian J. Duan; Shannon Dugan; Lauren A. Esposito; Markus Friedrich; Jessica Garb; Robin B. Gasser; Michael A.D. Goodisman; Dawn E. Gundersen-Rindal; Yi Han; Alfred M. Handler; Masatsugu Hatakeyama; Lars Hering; Wayne B. Hunter; Panagiotis Ioannidis; Joy C. Jayaseelan; Divya Kalra; Abderrahman Khila; Pasi K. Korhonen; Carol Eunmi Lee; Sandra L. Lee; Yiyuan Li; Amelia R.I. Lindsey; Georg Mayer; Alistair P. McGregor; Duane D. McKenna; Bernhard Misof; Mala Munidasa; Monica Munoz-Torres; Donna M. Muzny; Oliver Niehuis; Nkechinyere Osuji-Lacy; Subba R. Palli; Kristen A. Panfilio; Matthias Pechmann; Trent Perry; Ralph S. Peters; Helen C. Poynton; Nikola Michael Prpic; Jiaxin Qu; Dorith Rotenberg; Coby Schal; Sean D. Schoville; Erin D. Scully; Evette Skinner; Daniel B. Sloan; Richard Stouthamer; Michael R. Strand; Nikolaus U. Szucsich; Asela Wijeratne; Neil D. Young; Eduardo E. Zattara; Joshua B. Benoit; Evgeny M. Zdobnov; Michael E. Pfrender; Kevin J. Hackett; John H. Werren; Kim C. Worley; Richard A. Gibbs; Ariel D. Chipman; Robert M. Waterhouse; Erich Bornberg-Bauer; Matthew W. Hahn; Stephen Richards

doi:10.1186/s13059-019-1925-7

Gene content evolution in the arthropods

Gregg W.C. Thomas
, Elias Dohmen
, Daniel S.T. Hughes
, Shwetha C. Murali
, Monica Poelchau
, Karl Glastad
, Clare A. Anstead
, Nadia A. Ayoub
, Phillip Batterham
, Michelle Bellair
, Greta J. Binford
, Hsu Chao
, Yolanda H. Chen
, Christopher Childers
, Huyen Dinh
, Harsha Vardhan Doddapaneni
, Jian J. Duan
, Shannon Dugan
, Lauren A. Esposito
, Markus Friedrich

Jessica Garb, Robin B. Gasser, Michael A.D. Goodisman, Dawn E. Gundersen-Rindal, Yi Han, Alfred M. Handler, Masatsugu Hatakeyama, Lars Hering, Wayne B. Hunter, Panagiotis Ioannidis, Joy C. Jayaseelan, Divya Kalra, Abderrahman Khila, Pasi K. Korhonen, Carol Eunmi Lee, Sandra L. Lee, Yiyuan Li, Amelia R.I. Lindsey, Georg Mayer, Alistair P. McGregor, Duane D. McKenna, Bernhard Misof, Mala Munidasa, Monica Munoz-Torres, Donna M. Muzny, Oliver Niehuis, Nkechinyere Osuji-Lacy, Subba R. Palli, Kristen A. Panfilio, Matthias Pechmann, Trent Perry, Ralph S. Peters, Helen C. Poynton, Nikola Michael Prpic, Jiaxin Qu, Dorith Rotenberg, Coby Schal, Sean D. Schoville, Erin D. Scully, Evette Skinner, Daniel B. Sloan, Richard Stouthamer, Michael R. Strand, Nikolaus U. Szucsich, Asela Wijeratne, Neil D. Young, Eduardo E. Zattara, Joshua B. Benoit, Evgeny M. Zdobnov, Michael E. Pfrender, Kevin J. Hackett, John H. Werren, Kim C. Worley, Richard A. Gibbs, Ariel D. Chipman, Robert M. Waterhouse, Erich Bornberg-Bauer, Matthew W. Hahn, Stephen Richards

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

162 Scopus citations

Abstract

Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

Original language	English
Article number	15
Journal	Genome Biology
Volume	21
Issue number	1
DOIs	https://doi.org/10.1186/s13059-019-1925-7
State	Published - Jan 23 2020

Bibliographical note

Publisher Copyright:
© 2020 The Author(s).

Funding

Genome sequencing, assembly, and annotation were funded by National Human Genome Research Institute grant U54 HG003273 to R.A.G. GWCT and MWH are funded by NSF DBI-1564611. ED was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) 281125614 / GRK2220. RMW, PI, and EMZ were funded by The Swiss National Science Foundation (PP00P3_170664 to RMW, 31003A_143936 to EMZ). Contributions by DDM and AW were supported in part by NSF-DEB grant 1355169 and USDA-APHIS Cooperative Agreement 15-8130-0547-CA to DDM. BM and ON acknowledge the German Research foundation (NI 1387/3-1, MI 649/12-1) and the Leibnitz Graduate School on Genomic Biodiversity Research. CS was supported by the Blanton J. Whitmire endowment, Housing and Urban Development NCHHU-0007-13, National Science Foundation 1557864 and Alfred P. Sloan Foundation 2013-5-35 MBE. Funding from Australian Wool Innovation (to P.B. and R.B.G.) and the Australian Research Council (to R.B.G.) is gratefully acknowledged. Support to R.B.G.'s laboratory by YourGene Bioscience and Melbourne Water Corporation is gratefully acknowledged. This project was also supported by a Victorian Life Sciences Computation Initiative (VLSCI; grant number VR0007) on its Peak Computing Facility at the University of Melbourne, an initiative of the Victorian Government (R.B.G.). C.A.A. holds an NSERC Postdoctoral Fellowship. N.D.Y. holds an NHMRC Early Career Research Fellowship. P.K.K. is the recipient of a scholarship (STRAPA) from the University of Melbourne. No funding body participated in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Funders	Funder number
Australian Research Council
University of Melbourne
State Government of Victoria
Melbourne Water Corporation
Australian National Health and Medical Research Council
Natural Sciences and Engineering Research Council of Canada
Leibnitz Graduate School on Genomic Biodiversity Research
Alfred P Sloan Foundation
YourGene Bioscience
NSF-DEB-Award
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences	R01GM070559
USDA-APHIS	MI 649/12-1, 15-8130-0547-CA, NI 1387/3-1
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	PP00P3_170664, 170664, 31003A_143936, 143936
National Science Foundation Arctic Social Science Program	1557864, DBI-1564611, 1754190, 1355169
Blanton J. Whitmire Endowment	NCHHU-0007-13
UK Industrial Decarbonization Research and Innovation Centre	53706
Victorian Life Sciences Computation Initiative	VR0007
National Human Genome Research Institute	U54HG003273
Deutsche Forschungsgemeinschaft	281125614 / GRK2220
National Institute of Allergy and Infectious F32-AI286447 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI168214 Jason W. Rosch Diseases National Institute of Allergy and Infectious P30 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R00-AI166116 Christopher D. Radka Diseases National Institute of Allergy and Infectious T32-AI106700 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI192221 Jason W. Rosch Diseases National Inst...	R21AI131427

Keywords

Arthropods
DNA methylation
Evolution
Gene content
Genome assembly
Genomics
Protein domains

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
Cell Biology

Access to Document

10.1186/s13059-019-1925-7

Cite this

Thomas, G. W. C., Dohmen, E., Hughes, D. S. T., Murali, S. C., Poelchau, M., Glastad, K., Anstead, C. A., Ayoub, N. A., Batterham, P., Bellair, M., Binford, G. J., Chao, H., Chen, Y. H., Childers, C., Dinh, H., Doddapaneni, H. V., Duan, J. J., Dugan, S., Esposito, L. A., ... Richards, S. (2020). Gene content evolution in the arthropods. Genome Biology, 21(1), Article 15. https://doi.org/10.1186/s13059-019-1925-7

@article{9de1b1f2cd2c46c2b803ac446ac81d06,

title = "Gene content evolution in the arthropods",

abstract = "Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.",

keywords = "Arthropods, DNA methylation, Evolution, Gene content, Genome assembly, Genomics, Protein domains",

author = "Thomas, \{Gregg W.C.\} and Elias Dohmen and Hughes, \{Daniel S.T.\} and Murali, \{Shwetha C.\} and Monica Poelchau and Karl Glastad and Anstead, \{Clare A.\} and Ayoub, \{Nadia A.\} and Phillip Batterham and Michelle Bellair and Binford, \{Greta J.\} and Hsu Chao and Chen, \{Yolanda H.\} and Christopher Childers and Huyen Dinh and Doddapaneni, \{Harsha Vardhan\} and Duan, \{Jian J.\} and Shannon Dugan and Esposito, \{Lauren A.\} and Markus Friedrich and Jessica Garb and Gasser, \{Robin B.\} and Goodisman, \{Michael A.D.\} and Gundersen-Rindal, \{Dawn E.\} and Yi Han and Handler, \{Alfred M.\} and Masatsugu Hatakeyama and Lars Hering and Hunter, \{Wayne B.\} and Panagiotis Ioannidis and Jayaseelan, \{Joy C.\} and Divya Kalra and Abderrahman Khila and Korhonen, \{Pasi K.\} and Lee, \{Carol Eunmi\} and Lee, \{Sandra L.\} and Yiyuan Li and Lindsey, \{Amelia R.I.\} and Georg Mayer and McGregor, \{Alistair P.\} and McKenna, \{Duane D.\} and Bernhard Misof and Mala Munidasa and Monica Munoz-Torres and Muzny, \{Donna M.\} and Oliver Niehuis and Nkechinyere Osuji-Lacy and Palli, \{Subba R.\} and Panfilio, \{Kristen A.\} and Matthias Pechmann and Trent Perry and Peters, \{Ralph S.\} and Poynton, \{Helen C.\} and Prpic, \{Nikola Michael\} and Jiaxin Qu and Dorith Rotenberg and Coby Schal and Schoville, \{Sean D.\} and Scully, \{Erin D.\} and Evette Skinner and Sloan, \{Daniel B.\} and Richard Stouthamer and Strand, \{Michael R.\} and Szucsich, \{Nikolaus U.\} and Asela Wijeratne and Young, \{Neil D.\} and Zattara, \{Eduardo E.\} and Benoit, \{Joshua B.\} and Zdobnov, \{Evgeny M.\} and Pfrender, \{Michael E.\} and Hackett, \{Kevin J.\} and Werren, \{John H.\} and Worley, \{Kim C.\} and Gibbs, \{Richard A.\} and Chipman, \{Ariel D.\} and Waterhouse, \{Robert M.\} and Erich Bornberg-Bauer and Hahn, \{Matthew W.\} and Stephen Richards",

note = "Publisher Copyright: {\textcopyright} 2020 The Author(s).",

year = "2020",

month = jan,

day = "23",

doi = "10.1186/s13059-019-1925-7",

language = "English",

volume = "21",

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Thomas, GWC, Dohmen, E, Hughes, DST, Murali, SC, Poelchau, M, Glastad, K, Anstead, CA, Ayoub, NA, Batterham, P, Bellair, M, Binford, GJ, Chao, H, Chen, YH, Childers, C, Dinh, H, Doddapaneni, HV, Duan, JJ, Dugan, S, Esposito, LA, Friedrich, M, Garb, J, Gasser, RB, Goodisman, MAD, Gundersen-Rindal, DE, Han, Y, Handler, AM, Hatakeyama, M, Hering, L, Hunter, WB, Ioannidis, P, Jayaseelan, JC, Kalra, D, Khila, A, Korhonen, PK, Lee, CE, Lee, SL, Li, Y, Lindsey, ARI, Mayer, G, McGregor, AP, McKenna, DD, Misof, B, Munidasa, M, Munoz-Torres, M, Muzny, DM, Niehuis, O, Osuji-Lacy, N, Palli, SR, Panfilio, KA, Pechmann, M, Perry, T, Peters, RS, Poynton, HC, Prpic, NM, Qu, J, Rotenberg, D, Schal, C, Schoville, SD, Scully, ED, Skinner, E, Sloan, DB, Stouthamer, R, Strand, MR, Szucsich, NU, Wijeratne, A, Young, ND, Zattara, EE, Benoit, JB, Zdobnov, EM, Pfrender, ME, Hackett, KJ, Werren, JH, Worley, KC, Gibbs, RA, Chipman, AD, Waterhouse, RM, Bornberg-Bauer, E, Hahn, MW & Richards, S 2020, 'Gene content evolution in the arthropods', Genome Biology, vol. 21, no. 1, 15. https://doi.org/10.1186/s13059-019-1925-7

TY - JOUR

T1 - Gene content evolution in the arthropods

AU - Thomas, Gregg W.C.

AU - Dohmen, Elias

AU - Hughes, Daniel S.T.

AU - Murali, Shwetha C.

AU - Poelchau, Monica

AU - Glastad, Karl

AU - Anstead, Clare A.

AU - Ayoub, Nadia A.

AU - Batterham, Phillip

AU - Bellair, Michelle

AU - Binford, Greta J.

AU - Chao, Hsu

AU - Chen, Yolanda H.

AU - Childers, Christopher

AU - Dinh, Huyen

AU - Doddapaneni, Harsha Vardhan

AU - Duan, Jian J.

AU - Dugan, Shannon

AU - Esposito, Lauren A.

AU - Friedrich, Markus

AU - Garb, Jessica

AU - Gasser, Robin B.

AU - Goodisman, Michael A.D.

AU - Gundersen-Rindal, Dawn E.

AU - Han, Yi

AU - Handler, Alfred M.

AU - Hatakeyama, Masatsugu

AU - Hering, Lars

AU - Hunter, Wayne B.

AU - Ioannidis, Panagiotis

AU - Jayaseelan, Joy C.

AU - Kalra, Divya

AU - Khila, Abderrahman

AU - Korhonen, Pasi K.

AU - Lee, Carol Eunmi

AU - Lee, Sandra L.

AU - Li, Yiyuan

AU - Lindsey, Amelia R.I.

AU - Mayer, Georg

AU - McGregor, Alistair P.

AU - McKenna, Duane D.

AU - Misof, Bernhard

AU - Munidasa, Mala

AU - Munoz-Torres, Monica

AU - Muzny, Donna M.

AU - Niehuis, Oliver

AU - Osuji-Lacy, Nkechinyere

AU - Palli, Subba R.

AU - Panfilio, Kristen A.

AU - Pechmann, Matthias

AU - Perry, Trent

AU - Peters, Ralph S.

AU - Poynton, Helen C.

AU - Prpic, Nikola Michael

AU - Qu, Jiaxin

AU - Rotenberg, Dorith

AU - Schal, Coby

AU - Schoville, Sean D.

AU - Scully, Erin D.

AU - Skinner, Evette

AU - Sloan, Daniel B.

AU - Stouthamer, Richard

AU - Strand, Michael R.

AU - Szucsich, Nikolaus U.

AU - Wijeratne, Asela

AU - Young, Neil D.

AU - Zattara, Eduardo E.

AU - Benoit, Joshua B.

AU - Zdobnov, Evgeny M.

AU - Pfrender, Michael E.

AU - Hackett, Kevin J.

AU - Werren, John H.

AU - Worley, Kim C.

AU - Gibbs, Richard A.

AU - Chipman, Ariel D.

AU - Waterhouse, Robert M.

AU - Bornberg-Bauer, Erich

AU - Hahn, Matthew W.

AU - Richards, Stephen

PY - 2020/1/23

Y1 - 2020/1/23

N2 - Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

AB - Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

KW - Arthropods

KW - DNA methylation

KW - Evolution

KW - Gene content

KW - Genome assembly

KW - Genomics

KW - Protein domains

UR - https://www.scopus.com/pages/publications/85078222471

UR - https://www.scopus.com/pages/publications/85078222471#tab=citedBy

U2 - 10.1186/s13059-019-1925-7

DO - 10.1186/s13059-019-1925-7

M3 - Article

C2 - 31969194

AN - SCOPUS:85078222471

SN - 1474-7596

VL - 21

JO - Genome Biology

JF - Genome Biology

IS - 1

M1 - 15

ER -

Gene content evolution in the arthropods

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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