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Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

View ORCID ProfileAlice B. Dennis, Gabriel I. Ballesteros, Stéphanie Robin, Lukas Schrader, Jens Bast, Jan Berghöfer, Leo Beukeboom, Maya Belghazi, Anthony Bretaudeau, Jan Büllesbach, Elizabeth Cash, Dominique Colinet, Zoé Dumas, Patrizia Falabella, Jean-Luc Gatti, Elzemiek Geuverink, Joshua D. Gibson, Corinne Hertäg, Stefanie Hartmann, Emmanuelle Jacquin-Joly, Mark Lammers, Blas I. Lavandero, Ina Lindenbaum, Lauriane Massardier-Galata, Camille Meslin, Nicolas Montagné, Nina Pak, Marylène Poirié, Rosanna Salvia, Chris R. Smith, Denis Tagu, Sophie Tares, Heiko Vogel, Tanja Schwander, Jean-Christophe Simon, Christian C. Figueroa, Christoph Vorburger, Fabrice Legeai, Jürgen Gadau
doi: https://doi.org/10.1101/841288
Alice B. Dennis
1Department of Aquatic Ecology, Eawag, 8600 Dübendorf, Switzerland
2Institute of Integrative Biology, ETH Zürich, 8092 Zürich, Switzerland
3Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany
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  • ORCID record for Alice B. Dennis
  • For correspondence: alicebdennis@gmail.com
Gabriel I. Ballesteros
4Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile
5Centre for Molecular and Functional Ecology in Agroecosystems, Universidad de Talca, Talca, Chile
6Laboratorio de Control Biológico, Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile
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Stéphanie Robin
7IGEPP, Agrocampus Ouest, INRA, Université de Rennes, 35650 Le Rheu, France
8Université de Rennes 1, INRIA, CNRS, IRISA, 35000, Rennes, France
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Lukas Schrader
9Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany
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Jens Bast
10Department of Ecology and Evolution, Université de Lausanne, 1015 Lausanne
11Institute of Zoology, Universität zu Köln, 50674 Köln
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Jan Berghöfer
9Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany
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Leo Beukeboom
12Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands
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Maya Belghazi
13Aix-Marseille Univ, CNRS, INP, Inst Neurophysiopathol, PINT, PFNT, Marseille, France
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Anthony Bretaudeau
7IGEPP, Agrocampus Ouest, INRA, Université de Rennes, 35650 Le Rheu, France
8Université de Rennes 1, INRIA, CNRS, IRISA, 35000, Rennes, France
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Jan Büllesbach
9Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany
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Elizabeth Cash
14Department of Environmental Science, Policy, & Management, University of California, Berkeley, Berkeley, CA 94720, USA
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Dominique Colinet
15Université Côte d’Azur, INRA, CNRS, ISA, Sophia Antipolis, France
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Zoé Dumas
10Department of Ecology and Evolution, Université de Lausanne, 1015 Lausanne
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Patrizia Falabella
16University of Basilicata, Department of Sciences, 85100 Potenza, Italy
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Jean-Luc Gatti
15Université Côte d’Azur, INRA, CNRS, ISA, Sophia Antipolis, France
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Elzemiek Geuverink
12Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands
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Joshua D. Gibson
14Department of Environmental Science, Policy, & Management, University of California, Berkeley, Berkeley, CA 94720, USA
17Department of Biology, Georgia Southern University, Statesboro, GA 30460, USA
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Corinne Hertäg
18D-USYS, Department of Environmental Systems Sciences, ETH Zürich, Switzerland
1Department of Aquatic Ecology, Eawag, 8600 Dübendorf, Switzerland
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Stefanie Hartmann
3Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany
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Emmanuelle Jacquin-Joly
19INRA, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, F-78000 Versailles, France
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Mark Lammers
9Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany
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Blas I. Lavandero
6Laboratorio de Control Biológico, Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile
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Ina Lindenbaum
9Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany
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Lauriane Massardier-Galata
15Université Côte d’Azur, INRA, CNRS, ISA, Sophia Antipolis, France
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Camille Meslin
19INRA, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, F-78000 Versailles, France
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Nicolas Montagné
19INRA, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Diderot, Institute of Ecology and Environmental Sciences of Paris, iEES-Paris, F-78000 Versailles, France
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Nina Pak
14Department of Environmental Science, Policy, & Management, University of California, Berkeley, Berkeley, CA 94720, USA
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Marylène Poirié
15Université Côte d’Azur, INRA, CNRS, ISA, Sophia Antipolis, France
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Rosanna Salvia
16University of Basilicata, Department of Sciences, 85100 Potenza, Italy
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Chris R. Smith
20Department of Biology, Earlham College, Richmond, IN USA 47374
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Denis Tagu
7IGEPP, Agrocampus Ouest, INRA, Université de Rennes, 35650 Le Rheu, France
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Sophie Tares
15Université Côte d’Azur, INRA, CNRS, ISA, Sophia Antipolis, France
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Heiko Vogel
21Max Planck Institute for Chemical Ecology, Department of Entomology, Jena, Germany
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Tanja Schwander
10Department of Ecology and Evolution, Université de Lausanne, 1015 Lausanne
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Jean-Christophe Simon
7IGEPP, Agrocampus Ouest, INRA, Université de Rennes, 35650 Le Rheu, France
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Christian C. Figueroa
4Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile
5Centre for Molecular and Functional Ecology in Agroecosystems, Universidad de Talca, Talca, Chile
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Christoph Vorburger
1Department of Aquatic Ecology, Eawag, 8600 Dübendorf, Switzerland
2Institute of Integrative Biology, ETH Zürich, 8092 Zürich, Switzerland
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Fabrice Legeai
7IGEPP, Agrocampus Ouest, INRA, Université de Rennes, 35650 Le Rheu, France
8Université de Rennes 1, INRIA, CNRS, IRISA, 35000, Rennes, France
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Jürgen Gadau
9Institute for Evolution and Biodiversity, Universität Münster, Münster, Germany
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  • Abstract
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Abstract

Background Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts.

Results We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids’ endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids.

Conclusions These findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available at https://bipaa.genouest.org.

  • List of abbreviations

    A, T, C, G, and U
    Adenine, Thymine, Cytosine, Guanine, and Uracile, nucleotides
    bp
    Base Pair
    BIPAA
    BioInformatics Platform for Agroecosystem Arthropods (bipaa.genouest.org)
    BUSCO
    Benchmarking Universal Single-Copy Orthologs
    CDS
    Predicted Coding Sequence
    CSD
    Complementary Sex Determination
    CHC
    Cuticular Hydrocarbons
    DNMT
    DNA Methyltransferase genes
    CSP
    Chemosensory Protein
    GO
    Gene Ontology
    HMM
    Hidden Markov Model
    HOG
    Hierarchical Ortholog Group
    IR
    Ionotropic Receptor
    LRR
    Leucine Rich Repeat Proteins
    Mbp
    Mega Base Pairs, or 1,000,000bp
    MP
    Mate-pair sequence data
    NCBI
    National Center for Biotechnology Information
    N50
    A measure of genome completeness. The length of the scaffold containing the middle nucleotide
    OXPHOS
    Oxidative Phosphorylation
    OBP
    Odorant-binding Protein
    OR
    Odorant Receptor
    PE
    Paired-end sequence data
    RSCU
    Relative Synonymous Codon Usage
    TE
    Transposable Element
  • 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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    Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
    Alice B. Dennis, Gabriel I. Ballesteros, Stéphanie Robin, Lukas Schrader, Jens Bast, Jan Berghöfer, Leo Beukeboom, Maya Belghazi, Anthony Bretaudeau, Jan Büllesbach, Elizabeth Cash, Dominique Colinet, Zoé Dumas, Patrizia Falabella, Jean-Luc Gatti, Elzemiek Geuverink, Joshua D. Gibson, Corinne Hertäg, Stefanie Hartmann, Emmanuelle Jacquin-Joly, Mark Lammers, Blas I. Lavandero, Ina Lindenbaum, Lauriane Massardier-Galata, Camille Meslin, Nicolas Montagné, Nina Pak, Marylène Poirié, Rosanna Salvia, Chris R. Smith, Denis Tagu, Sophie Tares, Heiko Vogel, Tanja Schwander, Jean-Christophe Simon, Christian C. Figueroa, Christoph Vorburger, Fabrice Legeai, Jürgen Gadau
    bioRxiv 841288; doi: https://doi.org/10.1101/841288
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    Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum
    Alice B. Dennis, Gabriel I. Ballesteros, Stéphanie Robin, Lukas Schrader, Jens Bast, Jan Berghöfer, Leo Beukeboom, Maya Belghazi, Anthony Bretaudeau, Jan Büllesbach, Elizabeth Cash, Dominique Colinet, Zoé Dumas, Patrizia Falabella, Jean-Luc Gatti, Elzemiek Geuverink, Joshua D. Gibson, Corinne Hertäg, Stefanie Hartmann, Emmanuelle Jacquin-Joly, Mark Lammers, Blas I. Lavandero, Ina Lindenbaum, Lauriane Massardier-Galata, Camille Meslin, Nicolas Montagné, Nina Pak, Marylène Poirié, Rosanna Salvia, Chris R. Smith, Denis Tagu, Sophie Tares, Heiko Vogel, Tanja Schwander, Jean-Christophe Simon, Christian C. Figueroa, Christoph Vorburger, Fabrice Legeai, Jürgen Gadau
    bioRxiv 841288; doi: https://doi.org/10.1101/841288

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