A radiation of Psylliodes flea beetles on Brassicaceae is associated with the evolution of specific detoxification enzymes

Author:

Gikonyo Matilda W1,Ahn Seung-Joon12,Biondi Maurizio3,Fritzlar Frank4,Okamura Yu5ORCID,Vogel Heiko5,Köllner Tobias G6,Şen İsmail7,Hernández-Teixidor David8,Lee Chi-Feng9,Letsch Harald10ORCID,Beran Franziska1ORCID

Affiliation:

1. Research Group Sequestration and Detoxification in Insects, Max Planck Institute for Chemical Ecology , Jena , Germany

2. Department of Biochemistry, Molecular Biology, Entomology & Plant Pathology, Mississippi State University , Starkville, MS , US

3. Department of Life, Health and Environmental Sciences, University of L’Aquila , L’Aquila , Italy

4. Thüringer Landesamt für Umwelt, Bergbau und Naturschutz , Weimar , Germany

5. Department of Entomology, Max-Planck Institute for Chemical Ecology , Jena , Germany

6. Department of Natural Product Biosynthesis, Max-Planck Institute for Chemical Ecology , Jena , Germany

7. Faculty of Technology, Isparta University of Applied Sciences , Isparta , Turkey

8. Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC) , La Laguna, Tenerife, Canary Islands , Spain

9. Applied Zoology Division, Taiwan Agricultural Research Institute , Taichung , Taiwan

10. Department of Botany and Biodiversity Research, Division of Tropical Ecology and Animal Biodiversity, University of Vienna , Vienna , Austria

Abstract

Abstract Flea beetles of the genus Psylliodes have evolved specialized interactions with plant species belonging to several distantly related families, mainly Brassicaceae, Solanaceae, and Fagaceae. This diverse host use indicates that Psylliodes flea beetles are able to cope with different chemical defense metabolites, including glucosinolates, the characteristic defense metabolites of Brassicaceae. Here we investigated the evolution of host use and the emergence of a glucosinolate-specific detoxification mechanism in Psylliodes flea beetles. In phylogenetic analyses, Psylliodes species clustered into four major clades, three of which contained mainly species specialized on either Brassicaceae, Solanaceae, or Fagaceae. Most members of the fourth clade have broader host use, including Brassicaceae and Poaceae as major host plant families. Ancestral state reconstructions suggest that Psylliodes flea beetles were initially associated with Brassicaceae and then either shifted to Solanaceae or Fagaceae, or expanded their host repertoire to Poaceae. Despite a putative ancestral association with Brassicaceae, we found evidence that the evolution of glucosinolate-specific detoxification enzymes coincides with the radiation of Psylliodes on Brassicaceae, suggesting that these are not required for using Brassicaceae as hosts but could improve the efficiency of host use by specialized Psylliodes species.

Funder

Max Planck Society

International Max Planck Research School for Advanced Methods in Process and Systems Engineering

Daimler & Benz Foundation

German Federal Ministry for Education and Research

Publisher

Oxford University Press (OUP)

Subject

General Agricultural and Biological Sciences,Genetics,Ecology, Evolution, Behavior and Systematics

Reference101 articles.

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