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Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles

View ORCID ProfileMathieu Seppey, View ORCID ProfilePanagiotis Ioannidis, Brent C. Emerson, Camille Pitteloud, View ORCID ProfileMarc Robinson-Rechavi, View ORCID ProfileJulien Roux, Hermes E. Escalona, View ORCID ProfileDuane D. McKenna, Bernhard Misof, View ORCID ProfileSeunggwan Shin, View ORCID ProfileXin Zhou, View ORCID ProfileRobert M. Waterhouse, View ORCID ProfileNadir Alvarez
doi: https://doi.org/10.1101/399808
Mathieu Seppey
1Department of Ecology & Evolution, University of Lausanne, 1015 Lausanne, Switzerland
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  • ORCID record for Mathieu Seppey
Panagiotis Ioannidis
2Department of Genetic Medicine and Development, University of Geneva and Swiss Institute of Bioinformatics, Geneva, Switzerland
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Brent C. Emerson
3Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de la Laguna, Santa Cruz de Tenerife, Spain. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK
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Camille Pitteloud
4Department of Ecology & Evolution, University of Lausanne, 1015 Lausanne, Switzerland
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Marc Robinson-Rechavi
5Department of Ecology & Evolution, University of Lausanne, and Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
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Julien Roux
6Department of Ecology & Evolution, University of Lausanne, and Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
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Hermes E. Escalona
7Center for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig, Bonn, Germany
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Duane D. McKenna
8Department of Biological Sciences, University of Memphis, Memphis Tennessee, USA
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Bernhard Misof
9Center for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig, Bonn, Germany
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Seunggwan Shin
10Department of Biological Sciences, University of Memphis, Memphis Tennessee, USA
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Xin Zhou
11Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, China
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Robert M. Waterhouse
12Department of Ecology & Evolution, University of Lausanne, and Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
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Nadir Alvarez
13Department of Ecology & Evolution, University of Lausanne, 1015 Lausanne, Switzerland, and Museum of Natural History of the City of Geneva, Geneva, Switzerland
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Abstract

Background The diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed. Indeed the largest beetle suborder, Polyphaga, mostly includes plant-eaters among its ~315,000 species. In particular, plants defend themselves with a diversity of specialized toxic chemicals. These may impose selective pressures that drive genomic diversification and speciation in phytophagous beetles. However, evidence of changes in beetle gene repertoires driven by such interactions remains largely anecdotal and without explicit hypothesis testing.

Results To address this, we explored the genomic consequences of beetle-plant trophic interactions by performing comparative gene family analyses across 18 species representing the two most species-rich beetle suborders. We contrasted the gene contents of species from the mostly plant-eating suborder Polyphaga with those of the mainly predatory Adephaga. We found gene repertoire evolution to be more dynamic, with significantly more adaptive lineage-specific expansions, in the more speciose Polyphaga. Testing the specific hypothesis of adaptation to plant-feeding, we identified families of enzymes putatively involved in beetle-plant interactions that underwent adaptive expansions in Polyphaga. There was especially strong support for the selection hypothesis on large gene families for glutathione S-transferase and carboxylesterase detoxification enzymes.

Conclusions Our explicit modeling of the evolution of gene repertoires across 18 species identifies adaptive lineage-specific gene family expansions that accompany the dietary shift towards plants in beetles. These genomic signatures support the popular hypothesis of a key role for interactions with plant chemical defenses, and for plant-feeding in general, in driving beetle diversification.

Footnotes

  • Department of Genetic Medicine and Development, University of Geneva and Swiss Institute of Bioinformatics, Geneva, Switzerland.

  • Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology - Hellas, Heraklion, Greece.

  • Department of Environmental Systems Science, ETHZ, Zurich, Switzerland.

  • Department of Biomedicine, University of Basel, Basel, Switzerland.

  • mathieu.seppey{at}unige.ch, panagiotis_ioannidis{at}imbb.forth.gr, bemerson{at}ipna.csic.es, camille.pitteloud{at}usys.ethz.ch, marc.robinson-rechavi{at}unil.ch, julien.roux{at}unibas.ch, hermesescalona{at}gmail.com, dmckenna{at}memphis.edu, b.misof{at}zfmk.de, sshin4{at}memphis.edu, xinzhou{at}cau.edu.cn, robert.waterhouse{at}unil.ch, nadir.alvarez{at}ville-ge.ch

  • List of abbreviations

    ABC
    adenosine triphosphate-binding cassette transporters
    AICc
    Akaike Information Criterion (small-sample-size corrected)
    BM
    Brownian motion
    BUSCO
    Benchmarking Universal Single-Copy Ortholog assessment tool
    CAFE
    Computational Analysis of gene Family Evolution tool
    CE
    carboxylesterase
    CYS
    cysteine protease
    FDR
    false discovery rate
    GH
    glycoside hydrolase
    GST
    glutathione S-transferase
    LSE
    lineage specific expansion
    MAFFT
    Multiple Alignment using Fast Fourier Transform tool
    OG
    orthologous group
    OU
    Ornstein-Uhlenbeck
    P450
    cytochrome P450 monooxygenase
    SER
    serine protease
    UGT
    uridine 5’-diphospho-glycosyltransferase
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    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 4.0 International license.
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    Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles
    Mathieu Seppey, Panagiotis Ioannidis, Brent C. Emerson, Camille Pitteloud, Marc Robinson-Rechavi, Julien Roux, Hermes E. Escalona, Duane D. McKenna, Bernhard Misof, Seunggwan Shin, Xin Zhou, Robert M. Waterhouse, Nadir Alvarez
    bioRxiv 399808; doi: https://doi.org/10.1101/399808
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    Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles
    Mathieu Seppey, Panagiotis Ioannidis, Brent C. Emerson, Camille Pitteloud, Marc Robinson-Rechavi, Julien Roux, Hermes E. Escalona, Duane D. McKenna, Bernhard Misof, Seunggwan Shin, Xin Zhou, Robert M. Waterhouse, Nadir Alvarez
    bioRxiv 399808; doi: https://doi.org/10.1101/399808

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