Comprehensive Annotation of Olfactory and Gustatory Receptor Genes and Transposable Elements Revealed Their Evolutionary Dynamics in Aphids
Gene duplication and transposable elements (TEs) are major drivers of genomic innovation that can fuel adaptation. While the roles of duplication and TE-driven diversification are documented in plant pathogens, they remain insufficiently explored in insect pests such as aphids, where olfactory (OR) and gustatory receptor (GR) genes are key to host recognition. We analyzed 521 OR and 399 GR genes, alongside TEs, across 12 aphid genomes with varying host ranges. Aphid lineages with broader host ranges exhibited higher evolutionary rates, driven by gene family expansions linked to host interaction, including lipid metabolism, immune function, and transposase activity. OR and GR genes evolved through proximal and tandem duplications and were shaped by diversifying selection, with bursts of positive selection followed by prolonged purifying selection, consistent with adaptation to novel hosts. Younger TEs were significantly enriched near OR genes compared to GRs and other genomic regions, suggesting a catalytic role of TEs in their diversification. However, OR proteins encoded by TE-associated ORs exhibited reduced functional potential. In contrast, GR proteins encoded by TE-associated GRs retained signatures of adaptation, as inferred from deep learning models predicting functionally important protein regions. These findings suggest that TE activity may facilitate functional innovation in GRs while alleviating constraints or pseudogenization in ORs. This study reveals how duplication, selection, and TE dynamics shape gene evolution in insect pests. It also provides the first chromosome-scale genome assembly of Dysaphis plantaginea, with comprehensive annotations and functional predictions of OR/GR genes, bridging adaptive evolution with mechanistic insights.
Authors
- Yann Bourgeois (ORCID: https://orcid.org/0000-0002-1809-387X)
- Dominique Lavenier (ORCID: https://orcid.org/0000-0003-2557-680X)
- Amandine Cornille (ORCID: https://orcid.org/0000-0002-5348-7081)
- Sergio Gabriel Olvera-Vazquez
- Nicolas Francillonne
- Xilong Chen (ORCID: https://orcid.org/0000-0003-1588-6564)
- Stéphane Cauet (ORCID: https://orcid.org/0000-0003-4985-8940)
- Nathalie Rodde (ORCID: https://orcid.org/0000-0003-3361-4730)
- Emmanuelle Jacquin‐Joly (ORCID: https://orcid.org/0000-0002-6904-2036)
- Fabricio Almeida‐Silva (ORCID: https://orcid.org/0000-0002-5314-2964)
- Aurélie Mesnil (ORCID: https://orcid.org/0000-0002-8470-2610)
- Alessandra Carbone (ORCID: https://orcid.org/0000-0003-2098-5743)
- Claire Mottet (ORCID: https://orcid.org/0000-0001-8992-2383)
- Elorri Segura
- David Ogereau (ORCID: https://orcid.org/0000-0002-4496-3007)
- Camille Meslin (ORCID: https://orcid.org/0000-0003-2120-0936)
- Nathalie Choisne (ORCID: https://orcid.org/0000-0001-6024-1664)
- Karine Alix (ORCID: https://orcid.org/0000-0002-8133-0743)
- Johann Confais (ORCID: https://orcid.org/0000-0003-2945-5036)
- Fabrice Legeai (ORCID: https://orcid.org/0000-0002-6472-4839)
- Christelle Buchard
- Alexandre Degrave (ORCID: https://orcid.org/0000-0002-5642-3235)
- William Marande
- Gianluca Lombardi (ORCID: https://orcid.org/0009-0006-4183-5911)
- Jean-Christophe Simon
- B. Benoit
- Célia Lougmani
Institutions
- Université Claude Bernard Lyon 1 (FR)
- New York University Abu Dhabi (AE)
- Centre National de la Recherche Scientifique (FR)
- Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR)
- Institut Universitaire de France (FR)
- Université Paris-Est Créteil (FR)
- Université Paris Cité (FR)
- AgroParisTech (FR)
- Université Paris-Saclay (FR)
- Institut de Recherche en Informatique et Systèmes Aléatoires (FR)
- Ghent University (BE)
- Sorbonne Université (FR)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Biologie Computationnelle, Quantitative et Synthétique (FR)
- Génétique Quantitative et Évolution Le Moulon (FR)
- Évolution, Génomes, Comportement, Écologie (FR)
- Diversité, adaptation et développement des plantes (FR)
- Centre Inria de l'Université de Rennes (FR)
- Institut d'écologie et des sciences de l'environnement de Paris (FR)
- Laboratoire de Recherche en Sciences Végétales (FR)
- Institut de Génétique, Environnement et Protection des Plantes (FR)
- Laboratoire Ampère (FR)
- Institut de Recherche pour le Développement (FR)
- Université d'Angers (FR)
Publication Details
- Journal
- Molecular Biology and Evolution
- Published
- 2025-09-23
- DOI
- https://doi.org/10.1093/molbev/msaf238
- Primary Topic
- Insect-Plant Interactions and Control
- Type
- article
- Field-Weighted Citation Impact
- 0.00
Funders
- New York University Abu Dhabi
- York University
- Institut National de la Santé et de la Recherche Médicale
- Centre National de la Recherche Scientifique
- Université Paris-Saclay
- Tamkeen
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
- Institute of Genetics