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Gene content evolution in the arthropods

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 sequ...

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Autores principales: Thomas, Gregg W. C., Dohmen, Elias, Hughes, Daniel S. T., Murali, Shwetha C., Poelchau, Monica, Glastad, Karl, Anstead, Clare A., Ayoub, Nadia A., Batterham, Phillip, Bellair, Michelle, Binford, Greta J., Chao, Hsu, Chen, Yolanda H., Childers, Christopher, Dinh, Huyen, Doddapaneni, Harsha Vardhan, Duan, Jian J., Dugan, Shannon, Esposito, Lauren A., Friedrich, Markus, Garb, Jessica, Gasser, Robin B., Goodisman, Michael A. D., Gundersen-Rindal, Dawn E., Han, Yi, Handler, Alfred M., Hatakeyama, Masatsugu, Hering, Lars, Hunter, Wayne B., Ioannidis, Panagiotis, Jayaseelan, Joy C., Kalra, Divya, Khila, Abderrahman, Korhonen, Pasi K., Lee, Carol Eunmi, Lee, Sandra L., Li, Yiyuan, Lindsey, Amelia R. I., Mayer, Georg, McGregor, Alistair P., McKenna, Duane D., Misof, Bernhard, Munidasa, Mala, Munoz-Torres, Monica, Muzny, Donna M., Niehuis, Oliver, Osuji-Lacy, Nkechinyere, Palli, Subba R., Panfilio, Kristen A., Pechmann, Matthias, Perry, Trent, Peters, Ralph S., Poynton, Helen C., Prpic, Nikola-Michael, Qu, Jiaxin, Rotenberg, Dorith, Schal, Coby, Schoville, Sean D., Scully, Erin D., Skinner, Evette, Sloan, Daniel B., Stouthamer, Richard, Strand, Michael R., Szucsich, Nikolaus U., Wijeratne, Asela, Young, Neil D., Zattara, Eduardo E., Benoit, Joshua B., Zdobnov, Evgeny M., Pfrender, Michael E., Hackett, Kevin J., Werren, John H., Worley, Kim C., Gibbs, Richard A., Chipman, Ariel D., Waterhouse, Robert M., Bornberg-Bauer, Erich, Hahn, Matthew W., Richards, Stephen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6977273/
https://www.ncbi.nlm.nih.gov/pubmed/31969194
http://dx.doi.org/10.1186/s13059-019-1925-7
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author Thomas, Gregg W. C.
Dohmen, Elias
Hughes, Daniel S. T.
Murali, Shwetha C.
Poelchau, Monica
Glastad, Karl
Anstead, Clare A.
Ayoub, Nadia A.
Batterham, Phillip
Bellair, Michelle
Binford, Greta J.
Chao, Hsu
Chen, Yolanda H.
Childers, Christopher
Dinh, Huyen
Doddapaneni, Harsha Vardhan
Duan, Jian J.
Dugan, Shannon
Esposito, Lauren A.
Friedrich, Markus
Garb, Jessica
Gasser, Robin B.
Goodisman, Michael A. D.
Gundersen-Rindal, Dawn E.
Han, Yi
Handler, Alfred M.
Hatakeyama, Masatsugu
Hering, Lars
Hunter, Wayne B.
Ioannidis, Panagiotis
Jayaseelan, Joy C.
Kalra, Divya
Khila, Abderrahman
Korhonen, Pasi K.
Lee, Carol Eunmi
Lee, Sandra L.
Li, Yiyuan
Lindsey, Amelia R. I.
Mayer, Georg
McGregor, Alistair P.
McKenna, Duane D.
Misof, Bernhard
Munidasa, Mala
Munoz-Torres, Monica
Muzny, Donna M.
Niehuis, Oliver
Osuji-Lacy, Nkechinyere
Palli, Subba R.
Panfilio, Kristen A.
Pechmann, Matthias
Perry, Trent
Peters, Ralph S.
Poynton, Helen C.
Prpic, Nikola-Michael
Qu, Jiaxin
Rotenberg, Dorith
Schal, Coby
Schoville, Sean D.
Scully, Erin D.
Skinner, Evette
Sloan, Daniel B.
Stouthamer, Richard
Strand, Michael R.
Szucsich, Nikolaus U.
Wijeratne, Asela
Young, Neil D.
Zattara, Eduardo E.
Benoit, Joshua B.
Zdobnov, Evgeny M.
Pfrender, Michael E.
Hackett, Kevin J.
Werren, John H.
Worley, Kim C.
Gibbs, Richard A.
Chipman, Ariel D.
Waterhouse, Robert M.
Bornberg-Bauer, Erich
Hahn, Matthew W.
Richards, Stephen
author_facet Thomas, Gregg W. C.
Dohmen, Elias
Hughes, Daniel S. T.
Murali, Shwetha C.
Poelchau, Monica
Glastad, Karl
Anstead, Clare A.
Ayoub, Nadia A.
Batterham, Phillip
Bellair, Michelle
Binford, Greta J.
Chao, Hsu
Chen, Yolanda H.
Childers, Christopher
Dinh, Huyen
Doddapaneni, Harsha Vardhan
Duan, Jian J.
Dugan, Shannon
Esposito, Lauren A.
Friedrich, Markus
Garb, Jessica
Gasser, Robin B.
Goodisman, Michael A. D.
Gundersen-Rindal, Dawn E.
Han, Yi
Handler, Alfred M.
Hatakeyama, Masatsugu
Hering, Lars
Hunter, Wayne B.
Ioannidis, Panagiotis
Jayaseelan, Joy C.
Kalra, Divya
Khila, Abderrahman
Korhonen, Pasi K.
Lee, Carol Eunmi
Lee, Sandra L.
Li, Yiyuan
Lindsey, Amelia R. I.
Mayer, Georg
McGregor, Alistair P.
McKenna, Duane D.
Misof, Bernhard
Munidasa, Mala
Munoz-Torres, Monica
Muzny, Donna M.
Niehuis, Oliver
Osuji-Lacy, Nkechinyere
Palli, Subba R.
Panfilio, Kristen A.
Pechmann, Matthias
Perry, Trent
Peters, Ralph S.
Poynton, Helen C.
Prpic, Nikola-Michael
Qu, Jiaxin
Rotenberg, Dorith
Schal, Coby
Schoville, Sean D.
Scully, Erin D.
Skinner, Evette
Sloan, Daniel B.
Stouthamer, Richard
Strand, Michael R.
Szucsich, Nikolaus U.
Wijeratne, Asela
Young, Neil D.
Zattara, Eduardo E.
Benoit, Joshua B.
Zdobnov, Evgeny M.
Pfrender, Michael E.
Hackett, Kevin J.
Werren, John H.
Worley, Kim C.
Gibbs, Richard A.
Chipman, Ariel D.
Waterhouse, Robert M.
Bornberg-Bauer, Erich
Hahn, Matthew W.
Richards, Stephen
author_sort Thomas, Gregg W. C.
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13059-019-1925-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-69772732020-01-28 Gene content evolution in the arthropods Thomas, Gregg W. C. Dohmen, Elias Hughes, Daniel S. T. Murali, Shwetha C. Poelchau, Monica Glastad, Karl Anstead, Clare A. Ayoub, Nadia A. Batterham, Phillip Bellair, Michelle Binford, Greta J. Chao, Hsu Chen, Yolanda H. Childers, Christopher Dinh, Huyen Doddapaneni, Harsha Vardhan Duan, Jian J. Dugan, Shannon Esposito, Lauren A. Friedrich, Markus Garb, Jessica Gasser, Robin B. Goodisman, Michael A. D. Gundersen-Rindal, Dawn E. Han, Yi Handler, Alfred M. Hatakeyama, Masatsugu Hering, Lars Hunter, Wayne B. Ioannidis, Panagiotis Jayaseelan, Joy C. Kalra, Divya Khila, Abderrahman Korhonen, Pasi K. Lee, Carol Eunmi Lee, Sandra L. Li, Yiyuan Lindsey, Amelia R. I. Mayer, Georg McGregor, Alistair P. McKenna, Duane D. Misof, Bernhard Munidasa, Mala Munoz-Torres, Monica Muzny, Donna M. Niehuis, Oliver Osuji-Lacy, Nkechinyere Palli, Subba R. Panfilio, Kristen A. Pechmann, Matthias Perry, Trent Peters, Ralph S. Poynton, Helen C. Prpic, Nikola-Michael Qu, Jiaxin Rotenberg, Dorith Schal, Coby Schoville, Sean D. Scully, Erin D. Skinner, Evette Sloan, Daniel B. Stouthamer, Richard Strand, Michael R. Szucsich, Nikolaus U. Wijeratne, Asela Young, Neil D. Zattara, Eduardo E. Benoit, Joshua B. Zdobnov, Evgeny M. Pfrender, Michael E. Hackett, Kevin J. Werren, John H. Worley, Kim C. Gibbs, Richard A. Chipman, Ariel D. Waterhouse, Robert M. Bornberg-Bauer, Erich Hahn, Matthew W. Richards, Stephen Genome Biol Research 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13059-019-1925-7) contains supplementary material, which is available to authorized users. BioMed Central 2020-01-23 /pmc/articles/PMC6977273/ /pubmed/31969194 http://dx.doi.org/10.1186/s13059-019-1925-7 Text en © The Author(s). 2020 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Thomas, Gregg W. C.
Dohmen, Elias
Hughes, Daniel S. T.
Murali, Shwetha C.
Poelchau, Monica
Glastad, Karl
Anstead, Clare A.
Ayoub, Nadia A.
Batterham, Phillip
Bellair, Michelle
Binford, Greta J.
Chao, Hsu
Chen, Yolanda H.
Childers, Christopher
Dinh, Huyen
Doddapaneni, Harsha Vardhan
Duan, Jian J.
Dugan, Shannon
Esposito, Lauren A.
Friedrich, Markus
Garb, Jessica
Gasser, Robin B.
Goodisman, Michael A. D.
Gundersen-Rindal, Dawn E.
Han, Yi
Handler, Alfred M.
Hatakeyama, Masatsugu
Hering, Lars
Hunter, Wayne B.
Ioannidis, Panagiotis
Jayaseelan, Joy C.
Kalra, Divya
Khila, Abderrahman
Korhonen, Pasi K.
Lee, Carol Eunmi
Lee, Sandra L.
Li, Yiyuan
Lindsey, Amelia R. I.
Mayer, Georg
McGregor, Alistair P.
McKenna, Duane D.
Misof, Bernhard
Munidasa, Mala
Munoz-Torres, Monica
Muzny, Donna M.
Niehuis, Oliver
Osuji-Lacy, Nkechinyere
Palli, Subba R.
Panfilio, Kristen A.
Pechmann, Matthias
Perry, Trent
Peters, Ralph S.
Poynton, Helen C.
Prpic, Nikola-Michael
Qu, Jiaxin
Rotenberg, Dorith
Schal, Coby
Schoville, Sean D.
Scully, Erin D.
Skinner, Evette
Sloan, Daniel B.
Stouthamer, Richard
Strand, Michael R.
Szucsich, Nikolaus U.
Wijeratne, Asela
Young, Neil D.
Zattara, Eduardo E.
Benoit, Joshua B.
Zdobnov, Evgeny M.
Pfrender, Michael E.
Hackett, Kevin J.
Werren, John H.
Worley, Kim C.
Gibbs, Richard A.
Chipman, Ariel D.
Waterhouse, Robert M.
Bornberg-Bauer, Erich
Hahn, Matthew W.
Richards, Stephen
Gene content evolution in the arthropods
title Gene content evolution in the arthropods
title_full Gene content evolution in the arthropods
title_fullStr Gene content evolution in the arthropods
title_full_unstemmed Gene content evolution in the arthropods
title_short Gene content evolution in the arthropods
title_sort gene content evolution in the arthropods
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6977273/
https://www.ncbi.nlm.nih.gov/pubmed/31969194
http://dx.doi.org/10.1186/s13059-019-1925-7
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