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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
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  • For correspondence: kristen.panfilio@alum.swarthmore.edu
Iris M. Vargas Jentzsch
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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Joshua B. Benoit
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
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Deniz Erezyilmaz
4Department of Biochemistry and Cell Biology and Center for Developmental Genetics, Stony Brook University, Stony Brook, New York 11794, USA
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Yuichiro Suzuki
5Department of Biological Sciences, Wellesley College, 106 Central St., Wellesley, Massachusetts 02481, USA
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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
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Hugh M. Robertson
8Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA
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Monica F. Poelchau
9National Agricultural Library, Beltsville, Maryland 20705, USA
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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
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Panagiotis Ioannidis
10Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, Geneva 1211, Switzerland
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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
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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
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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
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John H. Werren
16Department of Biology, University of Rochester, Rochester, New York 14627, USA
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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
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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
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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
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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
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Patrice Baa-Puyoulet
6Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France
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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
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Chun-che Chang
23Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan
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Hsu Chao
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Mei-Ju M. Chen
9National Agricultural Library, Beltsville, Maryland 20705, USA
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Yen-Ta Chen
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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Christopher P. Childers
9National Agricultural Library, Beltsville, Maryland 20705, USA
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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
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Andrew G. Cridge
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
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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
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Peter K. Dearden
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
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Elise M. Didion
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
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Huyen Dinh
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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HarshaVardhan Doddapaneni
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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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
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Shannon Dugan
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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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
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Gérard Febvay
6Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France
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Markus Friedrich
27Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202, USA
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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
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Yi Han
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Peter Heger
28Institute for Genetics, University of Cologne, Zülpicher Straße 47a, 50674 Cologne, Germany
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Christopher J. Holmes
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
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Thorsten Horn
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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Yi-min Hsiao
23Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan
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Emily C. Jennings
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
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J. Spencer Johnston
29Department of Entomology, Texas A&M University, College Station, Texas 77843, USA
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Tamsin E. Jones
25Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA
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Jeffery W. Jones
27Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202, USA
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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
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Stefan Koelzer
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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Viera Kovacova
30CECAD, University of Cologne, Cologne, Germany
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Megan Leask
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
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Sandra L. Lee
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Chien-Yueh Lee
9National Agricultural Library, Beltsville, Maryland 20705, USA
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Mackenzie R. Lovegrove
19Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin 9054, New Zealand
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Hsiao-ling Lu
23Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan
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Yong Lu
31Department of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, Maryland 20742, USA
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Patricia J. Moore
32Department of Entomology, University of Georgia, 120 Cedar St., Athens, Georgia 30602, USA
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Monica C. Munoz-Torres
33Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Donna M. Muzny
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Subba R. Palli
34Department of Entomology, College of Agriculture, Food and Environment, University of Kentucky, Lexington, Kentucky 40546, USA
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Nicolas Parisot
6Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France
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Leslie Pick
31Department of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, Maryland 20742, USA
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Megan Porter
35Department of Biology, University of Hawai'i at Mānoa, Honolulu, Hawaii 96822, USA
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Jiaxin Qu
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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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
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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
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Rolando Rivera Pomar
38Centro de Bioinvestigaciones, Universidad Nacional del Noroeste de Buenos Aires, Argentina
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Andrew J. Rosendale
3Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221, USA
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Siegfried Roth
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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Lena Sachs
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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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
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Jan Seibert
1Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany
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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
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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
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Richard J. Stancliffe
40Argelander-Institut für Astronomie, Universität Bonn, Auf dem Hügel 71, 53121 Bonn, Germany
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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
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Lucila Traverso
42Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina
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Maurijn van der Zee
17Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands
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  • ORCID record for Maurijn van der Zee
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
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Kim C. Worley
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Evgeny M. Zdobnov
10Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, Geneva 1211, Switzerland
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Richard A. Gibbs
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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Stephen Richards
13Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA
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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.
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Posted October 31, 2018.
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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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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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