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 FriedrichJessica 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

128 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
Blanton J. Whitmire Endowment	NCHHU-0007-13
Leibnitz Graduate School on Genomic Biodiversity Research
Melbourne Water Corporation
NSF DEB-1655692	1355169
USDA-APHIS	MI 649/12-1, 15-8130-0547-CA, NI 1387/3-1
Victorian Life Sciences Computation Initiative	VR0007
YourGene Bioscience
National Science Foundation Arctic Social Science Program	1557864, DBI-1564611
National Science Foundation Arctic Social Science Program
National Human Genome Research Institute	U54 HG003273
National Human Genome Research Institute
National Institute of Allergy and Infectious Diseases	R21AI131427
National Institute of Allergy and Infectious Diseases
Alfred P Sloan Foundation
Natural Sciences and Engineering Research Council of Canada
Australian Research Council
Australian National Health and Medical Research Council
Deutsche Forschungsgemeinschaft	281125614 / GRK2220
Deutsche Forschungsgemeinschaft
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	PP00P3_170664, 31003A_143936
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
The University of Melbourne
State Government of Victoria

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

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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.",

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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

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DO - 10.1186/s13059-019-1925-7

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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

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