Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation

被引:104
作者
Dheilly, Nolwenn M. [1 ,2 ]
Maure, Fanny [2 ,3 ]
Ravallec, Marc [4 ]
Galinier, Richard [1 ]
Doyon, Josee [3 ]
Duval, David [1 ]
Leger, Lucas [2 ]
Volkoff, Anne-Nathalie [4 ]
Misse, Dorothee [2 ]
Nidelet, Sabine [5 ]
Demolombe, Vincent [5 ]
Brodeur, Jacques [3 ]
Gourbal, Benjamin [1 ]
Thomas, Frederic [2 ]
Mitta, Guillaume [1 ]
机构
[1] Univ Perpignan, CNRS, UMR 5244, 2EI, F-66860 Perpignan, France
[2] MIVEGEC UMR CNRS IRD UM1 UM2 5290, F-34394 Montpellier 5, France
[3] Univ Montreal, Inst Rech Biol Vegetale, Dept Sci Biol, Montreal, PQ H1X 2B2, Canada
[4] Univ Montpellier 2, INRA, UMR 1333, Insect Microorganisms Divers Genomes & Interact, F-34095 Montpellier, France
[5] MGX Montpellier GenomiX, Montpellier Genom & Bioinformat Facil, F-34396 Montpellier, France
关键词
parasitoid wasp; virus; holobiont; symbiont; behavioural manipulation; host-parasite interaction; CENTRAL NERVOUS-SYSTEM; STRANDED RNA VIRUSES; HEPATITIS-C VIRUS; ANTIVIRAL IMMUNITY; LIPID DROPLET; GLIAL REPAIR; MECHANISMS; HYMENOPTERA; AUTOPHAGY; INSECTS;
D O I
10.1098/rspb.2014.2773
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Many parasites modify their host behaviour to improve their own transmission and survival, but the proximate mechanisms remain poorly understood. An original model consists of the parasitoid Dinocampus coccinellae and its coccinellid host, Coleomegilla maculata; during the behaviour manipulation, the parasitoid is not in contact with its host anymore. We report herein the discovery and characterization of a new RNA virus of the parasitoid (D. coccinellae paralysis virus, DcPV). Using a combination of RT-qPCR and transmission electron microscopy, we demonstrate that DcPV is stored in the oviduct of parasitoid females, replicates in parasitoid larvae and is transmitted to the host during larval development. Next, DcPV replication in the host's nervous tissue induces a severe neuropathy and antiviral immune response that correlate with the paralytic symptoms characterizing the behaviour manipulation. Remarkably, virus clearance correlates with recovery of normal coccinellid behaviour. These results provide evidence that changes in ladybeetle behaviour most likely result from DcPV replication in the cerebral ganglia rather than by manipulation by the parasitoid. This offers stimulating prospects for research on parasitic manipulation by suggesting for the first time that behaviour manipulation could be symbiont-mediated.
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页数:10
相关论文
共 47 条
[31]   Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects [J].
Perrot-Minnot, Marie-Jeanne ;
Cezilly, Frank .
JOURNAL OF EXPERIMENTAL BIOLOGY, 2013, 216 (01) :134-141
[32]   Accurate Strand-Specific Quantification of Viral RNA [J].
Plaskon, Nicole E. ;
Adelman, Zach N. ;
Myles, Kevin M. .
PLOS ONE, 2009, 4 (10)
[33]   Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions [J].
Poulin, Robert .
ADVANCES IN THE STUDY OF BEHAVIOR, VOL 41, 2010, 41 :151-186
[34]   Presence of a novel small RNA-containing virus in a laboratory culture of the endoparasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae) [J].
Reineke, A ;
Asgari, S .
JOURNAL OF INSECT PHYSIOLOGY, 2005, 51 (02) :127-135
[35]   Behind Closed Membranes: The Secret Lives of Picornaviruses? [J].
Richards, Alexsia L. ;
Jackson, William T. .
PLOS PATHOGENS, 2013, 9 (05)
[36]   Autophagy in antiviral innate immunity [J].
Richetta, Clemence ;
Faure, Mathias .
CELLULAR MICROBIOLOGY, 2013, 15 (03) :368-376
[37]   Dicer-2 Processes Diverse Viral RNA Species [J].
Sabin, Leah R. ;
Zheng, Qi ;
Thekkat, Pramod ;
Yang, Jamie ;
Hannon, Gregory J. ;
Gregory, Brian D. ;
Tudor, Matthew ;
Cherry, Sara .
PLOS ONE, 2013, 8 (02)
[38]  
SMITH PJS, 1984, J NEUROSCI, V4, P2698
[39]  
SMITH PJS, 1987, J EXP BIOL, V132, P59
[40]   Exploring systemic RNA interference in insects:: a genome-wide survey for RNAi genes in Tribolium [J].
Tomoyasu, Yoshinori ;
Miller, Sherry C. ;
Tomita, Shuichiro ;
Schoppmeier, Michael ;
Grossmann, Daniela ;
Bucher, Gregor .
GENOME BIOLOGY, 2008, 9 (01)