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Abstract
Emergence of polyphagous herbivorous insects entails significant adaptation to recognize, detoxify and digest a variety of host-plants. Despite of its biological and practical importance - since insects eat 20% of crops - no exhaustive analysis of gene repertoires required for adaptations in generalist insect herbivores has previously been performed. The noctuid moth Spodoptera frugiperda ranks as one of the world’s worst agricultural pests. This insect is polyphagous while the majority of other lepidopteran herbivores are specialist. It consists of two morphologically indistinguishable strains (“C” and “R”) that have different host plant ranges. To describe the evolutionary mechanisms that both enable the emergence of polyphagous herbivory and lead to the shift in the host preference, we analyzed whole genome sequences from laboratory and natural populations of both strains. We observed huge expansions of genes associated with chemosensation and detoxification compared with specialist Lepidoptera. These expansions are largely due to tandem duplication, a possible adaptation mechanism enabling polyphagy. Individuals from natural C and R populations show significant genomic differentiation. We found signatures of positive selection in genes involved in chemoreception, detoxification and digestion, and copy number variation in the two latter gene families, suggesting an adaptive role for structural variation.
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1 INRIA, IRISA, GenScale, Campus de Beaulieu, Rennes, France
2 INRA, UMR Institut de Génétique, Environnement et Protection des Plantes (IGEPP), BioInformatics Platform for Agroecosystems Arthropods (BIPAA), Campus Beaulieu, Rennes, France; INRIA, IRISA, GenOuest Core Facility, Campus de Beaulieu, Rennes, France
3 DGIMI, INRA, Univ. Montpellier, Montpellier, France
4 CEA, Genoscope, 2 rue Gaston Crémieux, Evry, France
5 Université Côte d’Azur, INRA, CNRS, Institut Sophia Agrobiotech, 06903 Sophia-Antipolis, France
6 Sorbonne Universités, UPMC University Paris 06, Institute of Ecology and Environmental Sciences of Paris, Paris, France
7 Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany
8 URGI, INRA, Université Paris-Saclay, Versailles, France
9 School of Veterinary and Life Sciences, Murdoch University, Murdoch, Australia
10 INRA, Institute of Ecology and Environmental Sciences, Versailles, France; Laboratory of Mammalian Genetics, Center for DNA Fingerprinting and Diagnostics (CDFD), Lab block: Tuljaguda (Opp. MJ Market), Nampally, Hyderabad, India
11 Department of Genetics, Universitat de València, Burjassot, Valencia, Spain; Estructura de Recerca Interdisciplinar en Biotecnologia i Biomedicina (ERI-BIOTECMED), Universitat de València, Burjassot, Valencia, Spain
12 DGIMI, INRA, Univ. Montpellier, Montpellier, France; EPHE, PSL Research University, UMR1333 - DGIMI, Pathologie comparée des Invertébrés CC101, Montpellier cedex 5, France
13 Laboratory of Mammalian Genetics, Center for DNA Fingerprinting and Diagnostics (CDFD), Lab block: Tuljaguda (Opp. MJ Market), Nampally, Hyderabad, India
14 CSIRO Ecosystem Sciences, Black Mountain, Canberra, Australia
15 Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, Science Park 904, Amsterdam, The Netherlands
16 Plateforme MGX, C/o institut de Génomique Fonctionnelle, 141, rue de la Cardonille, Montpellier cedex 05, France
17 Key Laboratory of Forest Disaster Warning and Control of Yunnan Province, Southwest Forestry University, Kunming, China
18 INRA, Institute of Ecology and Environmental Sciences, Versailles, France
19 CSIRO, Clunies Ross St, (GPO Box 1700), Acton, Australia
20 Departamento de Entomologia e Acarologia, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, Av. Pádua Dias 11, Piracicaba, Brazil
21 Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, Pennsylvania, USA
22 Department of Plant Science, 102 Tyson Building, The Pennsylvania State University, University Park, Pennsylvania, USA
23 Department of Genetics, Universitat de València, Burjassot, Valencia, Spain
24 CEA, Genoscope, 2 rue Gaston Crémieux, Evry, France; CNRS UMR 8030, 2 rue Gaston Crémieux, Evry, France; Université d’Evry Val D’Essonne, Evry, France
25 INRA, UMR1062 CBGP, IRD, CIRAD, Montpellier SupAgro, 755 Avenue du campus Agropolis, Montferrier/Lez, France
26 Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany; Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, Science Park 904, Amsterdam, The Netherlands