A symbiotic gene stimulates aggressive behavior favoring the survival of parasitized caterpillars
Abstract
Animals often exhibit increased aggression in response to starvation, while parasites often manipulate host behavior. In contrast, underlying molecular mechanisms for these behavioral changes are mostly unknown. The diamondback moth, Plutella xylostella , is an agricultural pest that feeds on cruciferous plants as larvae, while Cotesia vestalis is a parasitoid wasp that parasitizes diamondback moth larvae. In this study, we determined that unparasitized diamondback moth larvae exhibit increased aggression and cannibalism when starved, while starved larvae parasitized by C. vestalis were more aggressive than unparasitized larvae. C. vestalis harbors a domesticated endogenized virus named Cotesia vestalis bracovirus (CvBV) that wasps inject into parasitized hosts. Starvation increased octopamine (OA) levels in the central nervous system (CNS) of diamondback moth larvae while a series of experiments identified a CvBV-encoded gene product named Assailant that further increased aggression in starved diamondback moth larvae. We determined that Assailant increases OA levels by activating tyramine beta-hydroxylase ( PxTβh ), which is a key enzyme in the OA biosynthesis pathway. Ectopic expression of assailant in Drosophila melanogaster likewise upregulated expression of DmTβh and OA, which increased aggressive behavior in male flies as measured by a well-established assay. While parasitized hosts are often thought to be at a competitive disadvantage to nonparasitized individuals, our results uncover how a parasitoid uses an endogenized virus to increase host aggression and enhance survival of offspring when competing against unparasitized hosts.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (19)
Zhiwei Wu
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Xiaotong Wu
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Zhizhi Wang
School of Life Science and Technology, ShanghaiTech University
Xiqian Ye
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Lan Pang
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Yanping Wang
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Yuenan Zhou
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Ting Chen
Sicong Zhou
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Zehua Wang
Department of Physics and Astronomy and the IQ Initiative
Yifeng Sheng
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Qichao Zhang
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Jiani Chen
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Pu Tang
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Xingxing Shen
Jianhua Huang
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University
Jean-Michel Drezen
Institut de Recherche sur la Biologie de l’Insecte, UMR 7261 CNRS - Université de Tours
Michael R. Strand
Department of Entomology, University of Georgia
Xuexin Chen
Zhejiang Engineering Research Center for Biological Control of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, State Key Lab of Rice Biology and Breeding, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University