Format

Send to

Choose Destination
Genome Biol. 2019 Apr 2;20(1):64. doi: 10.1186/s13059-019-1660-0.

Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome.

Author information

1
Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany. kristen.panfilio@alum.swarthmore.edu.
2
School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL, UK. kristen.panfilio@alum.swarthmore.edu.
3
Institute for Zoology: Developmental Biology, University of Cologne, Zülpicher Str. 47b, 50674, Cologne, Germany.
4
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
5
Department of Biochemistry and Cell Biology and Center for Developmental Genetics, Stony Brook University, Stony Brook, NY, 11794, USA.
6
Present address: Department of Physiology, Anatomy and Genetics and Centre for Neural Circuits and Behaviour, University of Oxford, Oxford, OX1 3SR, UK.
7
Department of Biological Sciences, Wellesley College, 106 Central St., Wellesley, MA, 02481, USA.
8
Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621, Villeurbanne, France.
9
Present address: LSTM, Laboratoire des Symbioses Tropicales et Méditerranéennes, INRA, IRD, CIRAD, SupAgro, University of Montpellier, Montpellier, France.
10
Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA.
11
National Agricultural Library, Beltsville, MD, 20705, USA.
12
Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.
13
Present address: Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.
14
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, Cincinnati, OH, 45229, USA.
15
Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
16
Present address: Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, 98195, USA.
17
Present address: Howard Hughes Medical Institute, University of Washington, Seattle, WA, 98195, USA.
18
Department of Biology, University of Rochester, Rochester, NY, 14627, USA.
19
Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE, Leiden, Netherlands.
20
Max Planck Institute for Chemical Ecology, Hans-Knöll Strasse 8, 07745, Jena, Germany.
21
Department of Biochemistry and Genomics Aotearoa, University of Otago, Dunedin, 9054, New Zealand.
22
School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, LS2 9JT, UK.
23
Institut 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.
24
Department 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.
25
Department of Entomology/Institute of Biotechnology, College of Bioresources and Agriculture, National Taiwan University, Taipei, Taiwan.
26
Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei, Taiwan.
27
Present address: School of Life Sciences, Rochester Institute of Technology, Rochester, NY, 14623, USA.
28
Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA.
29
Department of Molecular and Cellular Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA.
30
Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.
31
Institute for Genetics, University of Cologne, Zülpicher Straße 47a, 50674, Cologne, Germany.
32
Department of Entomology, Texas A&M University, College Station, TX, 77843, USA.
33
CECAD, University of Cologne, Cologne, Germany.
34
Department of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, MD, 20742, USA.
35
Department of Entomology, University of Georgia, 120 Cedar St., Athens, GA, 30602, USA.
36
Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
37
Department of Entomology, College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY, 40546, USA.
38
Department of Biology, University of Hawai'i at Mānoa, Honolulu, HI, 96822, USA.
39
Present address: Department of Evolutionary Genetics, Max-Planck-Institut für Evolutionsbiologie, August-Thienemann-Straße 2, 24306, Plön, Germany.
40
Present address: Earthworks Institute, 185 Caroline Street, Rochester, NY, 14620, USA.
41
Centro de Bioinvestigaciones, Universidad Nacional del Noroeste de Buenos Aires, Pergamino, Argentina.
42
Present address: Department of Biotechnology, Central University of Rajasthan (CURAJ), NH-8, Bandarsindri, Ajmer, 305801, India.
43
Argelander-Institut für Astronomie, Universität Bonn, Auf dem Hügel 71, 53121, Bonn, Germany.
44
Present address: E. A. Milne Centre for Astrophysics, Department of Physics and Mathematics, University of Hull, Hull, HU6 7RX, UK.
45
Present address: Department of Zoology, University of Cambridge, Cambridge, CB2 3DT, UK.
46
Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina.

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:

Evolution of development; Gene family evolution; Gene structure; Lateral gene transfer; Phytophagy; RNAi; Transcription factors

Supplemental Content

Full text links

Icon for BioMed Central Icon for PubMed Central
Loading ...
Support Center