Genome Biology (Apr 2019)
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,
- Harsha Vardhan 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 L. 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
Affiliations
- Kristen A. Panfilio
- Institute for Zoology: Developmental Biology, University of Cologne
- Iris M. Vargas Jentzsch
- Institute for Zoology: Developmental Biology, University of Cologne
- Joshua B. Benoit
- Department of Biological Sciences, University of Cincinnati
- Deniz Erezyilmaz
- Department of Biochemistry and Cell Biology and Center for Developmental Genetics, Stony Brook University
- Yuichiro Suzuki
- Department of Biological Sciences, Wellesley College
- Stefano Colella
- Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203
- Hugh M. Robertson
- Department of Entomology, University of Illinois at Urbana-Champaign
- Monica F. Poelchau
- National Agricultural Library
- Robert M. Waterhouse
- Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva
- Panagiotis Ioannidis
- Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva
- Matthew T. Weirauch
- Center 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
- Daniel S. T. Hughes
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Shwetha C. Murali
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- John H. Werren
- Department of Biology, University of Rochester
- Chris G. C. Jacobs
- Institute of Biology, Leiden University
- Elizabeth J. Duncan
- Department of Biochemistry and Genomics Aotearoa, University of Otago
- David Armisén
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Barbara M. I. Vreede
- Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem
- Patrice Baa-Puyoulet
- Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203
- Chloé S. Berger
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Chun-che Chang
- Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University
- Hsu Chao
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Mei-Ju M. Chen
- National Agricultural Library
- Yen-Ta Chen
- Institute for Zoology: Developmental Biology, University of Cologne
- Christopher P. Childers
- National Agricultural Library
- Ariel D. Chipman
- Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem
- Andrew G. Cridge
- Department of Biochemistry and Genomics Aotearoa, University of Otago
- Antonin J. J. Crumière
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Peter K. Dearden
- Department of Biochemistry and Genomics Aotearoa, University of Otago
- Elise M. Didion
- Department of Biological Sciences, University of Cincinnati
- Huyen Dinh
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Harsha Vardhan Doddapaneni
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Amanda Dolan
- Department of Biology, University of Rochester
- Shannon Dugan
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Cassandra G. Extavour
- Department of Organismic and Evolutionary Biology, Harvard University
- Gérard Febvay
- Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203
- Markus Friedrich
- Department of Biological Sciences, Wayne State University
- Neta Ginzburg
- Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem
- Yi Han
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Peter Heger
- Institute for Genetics, University of Cologne
- Christopher J. Holmes
- Department of Biological Sciences, University of Cincinnati
- Thorsten Horn
- Institute for Zoology: Developmental Biology, University of Cologne
- Yi-min Hsiao
- Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University
- Emily C. Jennings
- Department of Biological Sciences, University of Cincinnati
- J. Spencer Johnston
- Department of Entomology, Texas A&M University
- Tamsin E. Jones
- Department of Organismic and Evolutionary Biology, Harvard University
- Jeffery W. Jones
- Department of Biological Sciences, Wayne State University
- Abderrahman Khila
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Stefan Koelzer
- Institute for Zoology: Developmental Biology, University of Cologne
- Viera Kovacova
- CECAD, University of Cologne
- Megan Leask
- Department of Biochemistry and Genomics Aotearoa, University of Otago
- Sandra L. Lee
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Chien-Yueh Lee
- National Agricultural Library
- Mackenzie R. Lovegrove
- Department of Biochemistry and Genomics Aotearoa, University of Otago
- Hsiao-ling Lu
- Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University
- Yong Lu
- Department of Entomology and Program in Molecular & Cell Biology, University of Maryland
- Patricia J. Moore
- Department of Entomology, University of Georgia
- Monica C. Munoz-Torres
- Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory
- Donna M. Muzny
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Subba R. Palli
- Department of Entomology, College of Agriculture, Food and Environment, University of Kentucky
- Nicolas Parisot
- Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203
- Leslie Pick
- Department of Entomology and Program in Molecular & Cell Biology, University of Maryland
- Megan L. Porter
- Department of Biology, University of Hawai’i at Mānoa
- Jiaxin Qu
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Peter N. Refki
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Rose Richter
- Department of Biology, University of Rochester
- Rolando Rivera-Pomar
- Centro de Bioinvestigaciones, Universidad Nacional del Noroeste de Buenos Aires
- Andrew J. Rosendale
- Department of Biological Sciences, University of Cincinnati
- Siegfried Roth
- Institute for Zoology: Developmental Biology, University of Cologne
- Lena Sachs
- Institute for Zoology: Developmental Biology, University of Cologne
- M. Emília Santos
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Jan Seibert
- Institute for Zoology: Developmental Biology, University of Cologne
- Essia Sghaier
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Jayendra N. Shukla
- Department of Entomology, College of Agriculture, Food and Environment, University of Kentucky
- Richard J. Stancliffe
- Argelander-Institut für Astronomie, Universität Bonn
- Olivia Tidswell
- Department of Biochemistry and Genomics Aotearoa, University of Otago
- Lucila Traverso
- Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata
- Maurijn van der Zee
- Institute of Biology, Leiden University
- Séverine Viala
- Institut de Génomique Fonctionnelle de Lyon, Université de Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5242, École Normale Supérieure de Lyon
- Kim C. Worley
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Evgeny M. Zdobnov
- Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva
- Richard A. Gibbs
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- Stephen Richards
- Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine
- DOI
- https://doi.org/10.1186/s13059-019-1660-0
- Journal volume & issue
-
Vol. 20,
no. 1
pp. 1 – 26
Abstract
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 the 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.
Keywords
