Hostname: page-component-6d856f89d9-jhxnr Total loading time: 0 Render date: 2024-07-16T06:08:12.537Z Has data issue: false hasContentIssue false
  • English
  • Français

Deciphering the behaviour manipulation imposed by a virus on its parasitoid host: insights from a dual transcriptomic approach

Published online by Cambridge University Press:  28 May 2018

J. Varaldi Open the ORCID record for J. Varaldi [Opens in a new window]  and
D. Lepetit
J. Varaldi*
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive (UMR CNRS 5558), University Lyon 1 – University of Lyon, 43 boulevard du 11 novembre 1918, 69622 Villeurbanne cedex, France
D. Lepetit
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive (UMR CNRS 5558), University Lyon 1 – University of Lyon, 43 boulevard du 11 novembre 1918, 69622 Villeurbanne cedex, France
*
Author for correspondence: J. Varaldi, E-mail: julien.varaldi@univ-lyon1.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

Behaviour manipulation imposed by parasites is a fascinating phenomenon but our understanding is still very limited. We studied the interaction between a virus and the parasitic wasp Leptopilina boulardi that attacks Drosophila larvae. Wasps usually refrain to lay eggs into already parasitized hosts (superparasitism avoidance). On the contrary, females infected by the Leptopilina boulardi Filamentous Virus (LbFV) are much more incline to superparasitize. Interestingly, the host-sharing induced by this behaviour modification leads to the horizontal transmission of the virus, thus increasing its fitness at the expense of that of the wasp. To better understand the mechanisms underlying this behaviour manipulation, we studied by RNA sequencing the meta-transcriptome of LbFV and the parasitic wasp both in the abdomen and in the head. We found that the abundance of viral transcripts was independent of the wasp strain but strongly differed between tissues. Based on the tissue pattern of expression, we identified a set of 20 viral genes putatively involved in the manipulation process. In addition, we identified a set of wasp genes deregulated in the presence of the virus either in the abdomen or in the head, including genes with annotations suggesting involvement in behaviour (i.e. Potassium-channel protein). This dataset gives new insights into the behaviour manipulation and on the genetic basis of superparasitism in parasitoids.

Keywords

Behaviour manipulationGABAodorant receptorpotassium channelRNAseqsuperparasitismsymbiosis
Type
Research Article
Information
Parasitology , Volume 145 , Issue 14 , December 2018 , pp. 1979 - 1989
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anders, S, Pyl, PT and Huber, W (2015) HTSeq – a Python framework to work with high-throughput sequencing data. Bioinformatics (Oxford, England) 31, 166–169.Google Scholar
Barron, AB, Gurney, KN, Meah, LFS, Vasilaki, E and Marshall, JAR (2015) Decision-making and action selection in insects: inspiration from vertebrate-based theories. Frontiers in Behavioral Neuroscience 9, 363.Google Scholar
Bazellieres, E, Assemat, E, Arsanto, J-P, Le Bivic, A and Massey-Harroche, D (2009) Crumbs proteins in epithelial morphogenesis. Frontiers in Bioscience 14, 2149–2169.Google Scholar
Berdoy, M, Webster, JP and Macdonald, DW (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proceedings Biological Sciences/the Royal Society 267, 1591–1594.Google Scholar
Buttstedt, A, Moritz, RFA and Erler, S (2014) Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family. Biological Reviews 89, 255–269.Google Scholar
Charnov, EL (1976) Optimal foraging, the marginal value theorem. Theoretical Population Biology 9, 129–136.Google Scholar
Chen, YR, Zhong, S, Fei, Z, Hashimoto, Y, Xiang, JZ, Zhang, S and Blissard, GW (2013) The transcriptome of the baculovirus autographa californica multiple nucleopolyhedrovirus in trichoplusia ni cells. Journal of Virology 87, 6391–6405.Google Scholar
Cheung, SK and Scott, K (2017) GABAA receptor-expressing neurons promote consumption in Drosophila melanogaster. PLoS ONE 12, e0175177.Google Scholar
De Bary, HA (1879) De la symbiose. Revue internationale des Sciences 3, 301–309.Google Scholar
Finn, RD, Coggill, P, Eberhardt, RY, Eddy, SR, Mistry, J, Mitchell, AL, Potter, SC, Punta, M, Qureshi, M, Sangrador-Vegas, A, Salazar, GA, Tate, JG and Bateman, A (2016) The Pfam protein families database – towards a more sustainable future. Nucleic Acids Research 44, D279–D285.Google Scholar
Gandon, S, Rivero, A and Varaldi, J (2006) Superparasitism evolution: adaptation or manipulation? The American Naturalist 167, E1–E22.Google Scholar
Godfray, H (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ: Princeton University Press.Google Scholar
Han, Y, van Oers, MM, van Houte, S and Ros, VID (2015). Virus-induced behavioural changes in insects. In Mehlhorn, H (ed.), Host Manipulations by Parasites and Viruses. Cham: Springer International Publishing, pp. 149–174 doi: 10.1007/978-3-319-22936-2_10.Google Scholar
Hojo, M, Kagami, T, Sasaki, T, Nakamura, J and Sasaki, M (2010) Reduced expression of major royal jelly protein 1 gene in the mushroom bodies of worker honeybees with reduced learning ability. Apidologie 41, 194–202.Google Scholar
Hoover, K, Grove, M, Gardner, M, Hughes, DP, McNeil, J and Slavicek, J (2011) A gene for an extended phenotype. Science (New York, NY) 333, 1401.Google Scholar
Katsuma, S, Koyano, Y, Kang, W, Kokusho, R, Kamita, SG and Shimada, T (2012) The baculovirus uses a captured host phosphatase to induce enhanced locomotory activity in host caterpillars. PLoS Pathogens 8, e1002644.Google Scholar
Kim, D, Langmead, B and Salzberg, SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12, 357–360.Google Scholar
Leitão-Gonçalves, R, Carvalho-Santos, Z, Francisco, AP, Fioreze, GT, Anjos, M, Baltazar, C, Elias, AP, Itskov, PM, Piper, MDW and Ribeiro, C et al. (2017) Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLoS Biology 15, e2000862.Google Scholar
Lepetit, D, Gillet, B, Hughes, S, Kraaijeveld, K and Varaldi, J (2016) Genome sequencing of the behavior manipulating virus LbFV reveals a possible new virus family. Genome Biology and Evolution 8, 3718–3739.Google Scholar
Lodish, H, Berk, A, Zipursky, SL, Matsudaira, P, Baltimore, D and Darnell, D (2000) Molecular Cell Biology, 4th Edn. New York: W. H. Freeman.Google Scholar
Love, MI, Huber, W and Anders, S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 31.Google Scholar
Martinez, J, Fleury, F and Varaldi, J (2012a) Heritable variation in an extended phenotype: the case of a parasitoid manipulated by a virus. Journal of Evolutionary Biology 25, 54–65.Google Scholar
Martinez, J, Fleury, F and Varaldi, J (2015) Competitive outcome of multiple infections in a behavior-manipulating virus/wasp interaction. Ecology and Evolution 5(24), 5934–5945.Google Scholar
Martinez, J, Duplouy, A, Woolfit, M, Vavre, F, O'Neill, SL and Varaldi, J (2012b) Influence of the virus LbFV and of Wolbachia in a host-parasitoid interaction. PLoS ONE 7, e35081.Google Scholar
Miller, C (2000) An overview of the potassium channel family. Genome Biology 1(4), reviews0004.1–0004.5.Google Scholar
Palmer, MJ and Harvey, J (2014) Honeybee Kenyon cells are regulated by a tonic GABA receptor conductance. Journal of Neurophysiology 112, 2026–2035.Google Scholar
Palmgren, MG and Nissen, P (2011) P-Type ATPases. Annual Review of Biophysics 40, 243–266.Google Scholar
Patot, S, Lepetit, D, Charif, D, Varaldi, J and Fleury, F (2009) Molecular detection, penetrance, and transmission of an inherited virus responsible for behavioral manipulation of an insect parasitoid. Applied and Environmental Microbiology 75, 703–710.Google Scholar
Patot, S, Martinez, J, Allem, R, Gandon, S, Varaldi, J and Fleury, F (2010) Prevalence of a virus inducing behavioural manipulation near species range border. Molecular Ecology 19, 2995–3007.Google Scholar
Peixoto, LG, Calábria, LK, Garcia, L, Capparelli, FE, Goulart, LR, de Sousa, MV and et Espindola, FS (2009) Identification of major royal jelly proteins in the brain of the honeybee Apis mellifera. Journal of Insect Physiology 55, 671–677.Google Scholar
Peng, Y, Leung, HCM, Yiu, SM and Chin, FYL (2012) IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics (Oxford, England) 28, 1420–1428.Google Scholar
Pirri, JK, Rayes, D and Alkema, MJ (2015) A change in the ion selectivity of ligand-gated ion channels provides a mechanism to switch behavior. PLoS Biology 13, e1002238.Google Scholar
Ros, VID, van Houte, S, Hemerik, L and van Oers, MM (2015) Baculovirus-induced tree-top disease: how extended is the role of egt as a gene for the extended phenotype? Molecular Ecology 24, 249–258.Google Scholar
Ruschioni, S, van Loon, JJA, Smid, HM and van Lenteren, JC (2015) Insects can count: sensory basis of host discrimination in parasitoid wasps revealed. PLoS ONE 10, e0138045.Google Scholar
Simão, FA, Waterhouse, RM, Ioannidis, P, Kriventseva, EV and Zdobnov, EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics (Oxford, England) 31, 3210–3212.Google Scholar
Trapnell, C, Williams, BA, Pertea, G, Mortazavi, A, Kwan, G, van Baren, MJ, Salzberg, SL, Wold, BJ and Pachter, L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28, 511–515.Google Scholar
Van Alphen, JJ and Visser, ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35, 59–79.Google Scholar
Van Lenteren, JC and Bakker, K (1975) Discrimination between parasitised and unparasitised hosts in the parasitic wasp Pseudeucoila bochei: a matter of learning. Nature 254, 417–419.Google Scholar
Van Lenteren, JC, Ruschioni, S, Romani, R, Van Loon, JJA, Qiu, YT, Smid, HM, Isidoro, N and Bin, F (2007) Structure and electrophysiological responses of gustatory organs on the ovipositor of the parasitoid Leptopilina heterotoma. Arthropod Structure & Development 36, 271–276.Google Scholar
Varaldi, J, Fouillet, P, Ravallec, M, Lopez-Ferber, M, Boulétreau, M and Fleury, F (2003) Infectious behavior in a parasitoid. Science 302, 1930–1930.Google Scholar
Varaldi, J, Fouillet, P, Boulétreau, M and Fleury, F (2005) Superparasitism acceptance and patch-leaving mechanisms in parasitoids: a comparison between two sympatric wasps. Animal Behaviour 69, 1227–1234.Google Scholar
Varaldi, J, Ravallec, M, Labrosse, C, Lopez-Ferber, M, Boulétreau, M and Fleury, F (2006) Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp. Journal of Insect Physiology 52, 1202–1212.Google Scholar
Varaldi, J, Patot, S, Nardin, M and Gandon, S (2009) A virus-shaping reproductive strategy in a Drosophila parasitoid. Advances in Parasitology 70, 333–363.Google Scholar
Vieira, FG and Rozas, J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the arthropoda: origin and evolutionary history of the chemosensory system. Genome Biology and Evolution 3, 476–490.Google Scholar
Xue, W, Li, J-T, Zhu, Y-P, Hou, G-Y, Kong, X-F, Kuang, Y-Y and Sun, X-W (2013) L_RNA_scaffolder: scaffolding genomes with transcripts. BMC Genomics 14, 1–1.Google Scholar
Yang, C-H, Belawat, P, Hafen, E, Jan, LY, Jan, Y-N (2008) Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319, 1679–1683.Google Scholar
Supplementary material: File

Varaldi and Lepetit supplementary material

Varaldi and Lepetit supplementary material 1

Download Varaldi and Lepetit supplementary material(File)
File 1.5 MB