New Results
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome
View ORCID ProfileKristen A. Panfilio, View ORCID ProfileIris M. Vargas Jentzsch, View ORCID ProfileJoshua B. Benoit, View ORCID ProfileDeniz Erezyilmaz, View ORCID ProfileYuichiro Suzuki, View ORCID ProfileStefano Colella, Hugh M. Robertson, View ORCID ProfileMonica F. Poelchau, View ORCID ProfileRobert M. Waterhouse, View ORCID ProfilePanagiotis Ioannidis, View ORCID ProfileMatthew T. Weirauch, Daniel S.T. Hughes, Shwetha C. Murali, View ORCID ProfileJohn H. Werren, View ORCID ProfileChris G.C. Jacobs, View ORCID ProfileElizabeth J. Duncan, David Armisén, View ORCID ProfileBarbara M.I. Vreede, Patrice Baa-Puyoulet, Chloé S. Berger, View ORCID ProfileChun-che Chang, Hsu Chao, View ORCID ProfileMei-Ju M. Chen, Yen-Ta Chen, View ORCID ProfileChristopher P. Childers, View ORCID ProfileAriel D. Chipman, View ORCID ProfileAndrew G. Cridge, Antonin J.J. Crumière, View ORCID ProfilePeter K. Dearden, View ORCID ProfileElise M. Didion, View ORCID ProfileHuyen Dinh, View ORCID ProfileHarshaVardhan Doddapaneni, Amanda Dolan, View ORCID ProfileShannon Dugan, View ORCID ProfileCassandra G. Extavour, View ORCID ProfileGérard Febvay, View ORCID ProfileMarkus Friedrich, Neta Ginzburg, View ORCID ProfileYi Han, Peter Heger, View ORCID ProfileChristopher J. Holmes, View ORCID ProfileThorsten Horn, View ORCID ProfileYi-min Hsiao, View ORCID ProfileEmily C. Jennings, View ORCID ProfileJ. Spencer Johnston, Tamsin E. Jones, Jeffery W. Jones, View ORCID ProfileAbderrahman Khila, Stefan Koelzer, View ORCID ProfileViera Kovacova, Megan Leask, View ORCID ProfileSandra L. Lee, Chien-Yueh Lee, Mackenzie R. Lovegrove, Hsiao-ling Lu, Yong Lu, View ORCID ProfilePatricia J. Moore, View ORCID ProfileMonica C. Munoz-Torres, View ORCID ProfileDonna M. Muzny, View ORCID ProfileSubba R. Palli, View ORCID ProfileNicolas Parisot, View ORCID ProfileLeslie Pick, View ORCID ProfileMegan Porter, View ORCID ProfileJiaxin Qu, Peter N. Refki, Rose Richter, View ORCID ProfileRolando Rivera Pomar, View ORCID ProfileAndrew J. Rosendale, View ORCID ProfileSiegfried Roth, Lena Sachs, M. Emília Santos, Jan Seibert, Essia Sghaier, View ORCID ProfileJayendra N. Shukla, View ORCID ProfileRichard J. Stancliffe, Olivia Tidswell, Lucila Traverso, View ORCID ProfileMaurijn van der Zee, Séverine Viala, View ORCID ProfileKim C. Worley, Evgeny M. Zdobnov, Richard A. Gibbs, View ORCID ProfileStephen Richards
doi: https://doi.org/10.1101/201731
Kristen A. Panfilio
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
2School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry CV4 7AL, UK
Iris M. Vargas Jentzsch
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
Joshua B. Benoit
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
Deniz Erezyilmaz
4Department of Biochemistry and Cell Biology and Center for Developmental Genetics, Stony Brook University, Stony Brook, New York 11794, USA
Yuichiro Suzuki
5Department of Biological Sciences, Wellesley College, 106 Central St., Wellesley, Massachusetts 02481, USA
Stefano Colella
6Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France
7Current address: LSTM, Laboratoire des Symbioses Tropicales et Méditerranéennes, INRA, IRD, CIRAD, SupAgro, University of Montpellier, Montpellier, France
Hugh M. Robertson
8Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA
Monica F. Poelchau
9National Agricultural Library, Beltsville, Maryland 20705, USA
Robert M. Waterhouse
10Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, Geneva 1211, Switzerland
11Current address: Department of Ecology and Evolution, University of Lausanne, Lausanne 1015, Switzerland
Panagiotis Ioannidis
10Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, Geneva 1211, Switzerland
Matthew T. Weirauch
12Center for Autoimmune Genomics and Etiology, Division of Biomedical Informatics, and Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Department of Pediatrics, College of Medicine, University of Cincinnati, Cincinnati, Ohio 45229, USA
Daniel S.T. Hughes
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Shwetha C. Murali
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
14Current address: Department of Genome Sciences, University of Washington School of Medicine, Seattle, Washington 98195, USA
15Current address: Howard Hughes Medical Institute, University of Washington, Seattle, Washington 98195, USA
John H. Werren
16Department of Biology, University of Rochester, Rochester, New York 14627, USA
Chris G.C. Jacobs
17Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands
18Max Planck Institute for Chemical Ecology, Hans-Knöll Strasse 8, 07745 Jena, Germany
Elizabeth J. Duncan
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
20School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK
David Armisén
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
Barbara M.I. Vreede
22Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram 91904, Jerusalem, Israel
Patrice Baa-Puyoulet
6Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France
Chloé S. Berger
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
Chun-che Chang
23Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan
Hsu Chao
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Mei-Ju M. Chen
9National Agricultural Library, Beltsville, Maryland 20705, USA
Yen-Ta Chen
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
Christopher P. Childers
9National Agricultural Library, Beltsville, Maryland 20705, USA
Ariel D. Chipman
22Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram 91904, Jerusalem, Israel
Andrew G. Cridge
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
Antonin J.J. Crumière
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
Peter K. Dearden
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
Elise M. Didion
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
Huyen Dinh
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
HarshaVardhan Doddapaneni
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Amanda Dolan
16Department of Biology, University of Rochester, Rochester, New York 14627, USA
24Current address: School of Life Sciences, Rochester Institute of Technology, Rochester, New York 14623, USA
Shannon Dugan
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Cassandra G. Extavour
25Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA
26Department of Molecular and Cellular Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA
Gérard Febvay
6Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France
Markus Friedrich
27Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202, USA
Neta Ginzburg
22Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram 91904, Jerusalem, Israel
Yi Han
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Peter Heger
28Institute for Genetics, University of Cologne, Zülpicher Straße 47a, 50674 Cologne, Germany
Christopher J. Holmes
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
Thorsten Horn
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
Yi-min Hsiao
23Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan
Emily C. Jennings
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
J. Spencer Johnston
29Department of Entomology, Texas A&M University, College Station, Texas 77843, USA
Tamsin E. Jones
25Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA
Jeffery W. Jones
27Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202, USA
Abderrahman Khila
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
Stefan Koelzer
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
Viera Kovacova
30CECAD, University of Cologne, Cologne, Germany
Megan Leask
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
Sandra L. Lee
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Chien-Yueh Lee
9National Agricultural Library, Beltsville, Maryland 20705, USA
Mackenzie R. Lovegrove
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
Hsiao-ling Lu
23Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan
Yong Lu
31Department of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, Maryland 20742, USA
Patricia J. Moore
32Department of Entomology, University of Georgia, 120 Cedar St., Athens, Georgia 30602, USA
Monica C. Munoz-Torres
33Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA
Donna M. Muzny
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Subba R. Palli
34Department of Entomology, College of Agriculture, Food and Environment, University of Kentucky, Lexington, Kentucky 40546, USA
Nicolas Parisot
6Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France
Leslie Pick
31Department of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, Maryland 20742, USA
Megan Porter
35Department of Biology, University of Hawai'i at Mānoa, Honolulu, Hawaii 96822, USA
Jiaxin Qu
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Peter N. Refki
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
36Current address: Department of Evolutionary Genetics, Max-Planck-Institut für Evolutionsbiologie, August-Thienemann-Straße 2, 24306 Plön, Germany
Rose Richter
16Department of Biology, University of Rochester, Rochester, New York 14627, USA
37Current address: Earthworks Institute, 185 Caroline Street, Rochester, New York 14620, USA
Rolando Rivera Pomar
38Centro de Bioinvestigaciones, Universidad Nacional del Noroeste de Buenos Aires, Argentina
Andrew J. Rosendale
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
Siegfried Roth
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
Lena Sachs
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
M. Emília Santos
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
Jan Seibert
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
Essia Sghaier
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
Jayendra N. Shukla
34Department of Entomology, College of Agriculture, Food and Environment, University of Kentucky, Lexington, Kentucky 40546, USA
39Current address: Department of Biotechnology, Central university of Rajasthan (CURAJ), NH-8, Bandarsindri, Ajmer-305801, India
Richard J. Stancliffe
40Argelander-Institut für Astronomie, Universität Bonn, Auf dem Hügel 71, 53121 Bonn, Germany
Olivia Tidswell
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
41Current address: Department of Zoology, University of Cambridge, Cambridge CB2 3DT, UK
Lucila Traverso
42Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina
Maurijn van der Zee
17Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands
Séverine Viala
21Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon, 46 Allée d'Italie, 69364 Lyon, France
Kim C. Worley
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Evgeny M. Zdobnov
10Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, Geneva 1211, Switzerland
Richard A. Gibbs
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Stephen Richards
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
Abstract
Background The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae.
Results The 926-Mb Oncopeltus genome is well represented by the current assembly and official gene set. We use our genomic and RNA-seq data not only to characterize the protein-coding gene repertoire and perform isoform-specific RNAi, but also to elucidate patterns of molecular evolution and physiology. We find ongoing, lineage-specific expansion and diversification of repressive C2H2 zinc finger proteins. The discovery of intron gain and turnover specific to the Hemiptera also prompted evaluation of lineage and genome size as predictors of gene structure evolution. Furthermore, we identify enzymatic gains and losses that correlate with feeding biology, particularly for reductions associated with derived, fluid-nutrition feeding.
Conclusions With the milkweed bug, we now have a critical mass of sequenced species for a hemimetabolous insect order and close outgroup to the Holometabola, substantially improving the diversity of insect genomics. We thereby define commonalities among the Hemiptera and delve into how hemipteran genomes reflect distinct feeding ecologies. Given Oncopeltus's strength as an experimental model, these new sequence resources bolster the foundation for molecular research and highlight technical considerations for the analysis of medium-sized invertebrate genomes.
Copyright
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
Posted October 31, 2018.
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome
Kristen A. Panfilio, Iris M. Vargas Jentzsch, Joshua B. Benoit, Deniz Erezyilmaz, Yuichiro Suzuki, Stefano Colella, Hugh M. Robertson, Monica F. Poelchau, Robert M. Waterhouse, Panagiotis Ioannidis, Matthew T. Weirauch, Daniel S.T. Hughes, Shwetha C. Murali, John H. Werren, Chris G.C. Jacobs, Elizabeth J. Duncan, David Armisén, Barbara M.I. Vreede, Patrice Baa-Puyoulet, Chloé S. Berger, Chun-che Chang, Hsu Chao, Mei-Ju M. Chen, Yen-Ta Chen, Christopher P. Childers, Ariel D. Chipman, Andrew G. Cridge, Antonin J.J. Crumière, Peter K. Dearden, Elise M. Didion, Huyen Dinh, HarshaVardhan Doddapaneni, Amanda Dolan, Shannon Dugan, Cassandra G. Extavour, Gérard Febvay, Markus Friedrich, Neta Ginzburg, Yi Han, Peter Heger, Christopher J. Holmes, Thorsten Horn, Yi-min Hsiao, Emily C. Jennings, J. Spencer Johnston, Tamsin E. Jones, Jeffery W. Jones, Abderrahman Khila, Stefan Koelzer, Viera Kovacova, Megan Leask, Sandra L. Lee, Chien-Yueh Lee, Mackenzie R. Lovegrove, Hsiao-ling Lu, Yong Lu, Patricia J. Moore, Monica C. Munoz-Torres, Donna M. Muzny, Subba R. Palli, Nicolas Parisot, Leslie Pick, Megan Porter, Jiaxin Qu, Peter N. Refki, Rose Richter, Rolando Rivera Pomar, Andrew J. Rosendale, Siegfried Roth, Lena Sachs, M. Emília Santos, Jan Seibert, Essia Sghaier, Jayendra N. Shukla, Richard J. Stancliffe, Olivia Tidswell, Lucila Traverso, Maurijn van der Zee, Séverine Viala, Kim C. Worley, Evgeny M. Zdobnov, Richard A. Gibbs, Stephen Richards
bioRxiv 201731; doi: https://doi.org/10.1101/201731
Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome
Kristen A. Panfilio, Iris M. Vargas Jentzsch, Joshua B. Benoit, Deniz Erezyilmaz, Yuichiro Suzuki, Stefano Colella, Hugh M. Robertson, Monica F. Poelchau, Robert M. Waterhouse, Panagiotis Ioannidis, Matthew T. Weirauch, Daniel S.T. Hughes, Shwetha C. Murali, John H. Werren, Chris G.C. Jacobs, Elizabeth J. Duncan, David Armisén, Barbara M.I. Vreede, Patrice Baa-Puyoulet, Chloé S. Berger, Chun-che Chang, Hsu Chao, Mei-Ju M. Chen, Yen-Ta Chen, Christopher P. Childers, Ariel D. Chipman, Andrew G. Cridge, Antonin J.J. Crumière, Peter K. Dearden, Elise M. Didion, Huyen Dinh, HarshaVardhan Doddapaneni, Amanda Dolan, Shannon Dugan, Cassandra G. Extavour, Gérard Febvay, Markus Friedrich, Neta Ginzburg, Yi Han, Peter Heger, Christopher J. Holmes, Thorsten Horn, Yi-min Hsiao, Emily C. Jennings, J. Spencer Johnston, Tamsin E. Jones, Jeffery W. Jones, Abderrahman Khila, Stefan Koelzer, Viera Kovacova, Megan Leask, Sandra L. Lee, Chien-Yueh Lee, Mackenzie R. Lovegrove, Hsiao-ling Lu, Yong Lu, Patricia J. Moore, Monica C. Munoz-Torres, Donna M. Muzny, Subba R. Palli, Nicolas Parisot, Leslie Pick, Megan Porter, Jiaxin Qu, Peter N. Refki, Rose Richter, Rolando Rivera Pomar, Andrew J. Rosendale, Siegfried Roth, Lena Sachs, M. Emília Santos, Jan Seibert, Essia Sghaier, Jayendra N. Shukla, Richard J. Stancliffe, Olivia Tidswell, Lucila Traverso, Maurijn van der Zee, Séverine Viala, Kim C. Worley, Evgeny M. Zdobnov, Richard A. Gibbs, Stephen Richards
bioRxiv 201731; doi: https://doi.org/10.1101/201731
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