Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T04:24:50.976Z Has data issue: false hasContentIssue false
  • English
  • Français

Timely trigger of caterpillar zombie behaviour: temporal requirements for light in baculovirus-induced tree-top disease

Published online by Cambridge University Press:  16 November 2017

Yue Han ,
Stineke van Houte ,
Monique M. van Oers  and
Vera I. D. Ros Open the ORCID record for Vera I. D. Ros [Opens in a new window]
Yue Han
Affiliation:
Laboratory of Virology, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Stineke van Houte
Affiliation:
Laboratory of Virology, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands Centre for Ecology and Conservation, Biosciences, University of Exeter, Penryn, Cornwall TR10 9FE, UK
Monique M. van Oers
Affiliation:
Laboratory of Virology, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Vera I. D. Ros*
Affiliation:
Laboratory of Virology, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
*
Author for correspondence: Vera I. D. Ros, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Host behavioural manipulation is a common strategy used by parasites to enhance their survival and/or transmission. Baculoviruses induce hyperactivity and tree-top disease (pre-death climbing behaviour) in their caterpillar hosts. However, little is known about the underlying mechanisms of this behavioural manipulation. A previous study showed that the baculovirus Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) induced tree-top disease at 3 days post infection in third instar S. exigua larvae and that light plays a key role in triggering this behaviour. Here we investigated the temporal requirements for the presence of light to trigger this behaviour and found that light from above was needed between 43 and 50 h post infection to induce tree-top disease. Infected larvae that were not exposed to light from above in this period finally died at low positions. Exposure to light prior to this period did not affect the final positions where larvae died. Overall we conclude that light in a particular time frame is needed to trigger SeMNPV-induced tree-top disease in S. exigua larvae.

Keywords

Behavioural manipulationparasitic manipulationtree-top diseasebaculovirusSeMNPVSpodoptera exiguaphototaxis
Type
Research Article
Information
Parasitology , Volume 145 , Issue 6 , May 2018 , pp. 822 - 827
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Benesh, DP, Duclos, LM and Nickol, BB (2005) The behavioral response of amphipods harboring Corynosoma constrictum (Acanthocephala) to various components of light. Journal of Parasitology 91, 731–736.Google Scholar
Biron, DG, Ponton, F, Marche, L, Galeotti, N, Renault, L, Demey-Thomas, E, Poncet, J, Brown, SP, Jouin, P and Thomas, F (2006) ‘Suicide’ of crickets harboring hairworms: a proteomics investigation. Insect Molecular Biology 15, 731–742.Google Scholar
Bos, N, Lefèvre, T, Jensen, AB and d'Ettorre, P (2012) Sick ants become unsociable. Journal of Evolutionary Biology 25, 342–351.Google Scholar
Castrejon, F and Rojas, JC (2010) Behavioral responses of larvae and adults of Estigmene acrea (Lepidoptera: Arctiidae) to light of different wavelengths. Florida Entomologist 93, 505–509.Google Scholar
Chung, TY, Sun, PF, Kuo, JI, Lee, YI, Lin, CC and Chou, JY (2017) Zombie ant heads are oriented relative to solar cues. Fungal Ecology 25, 22–28.Google Scholar
Fischbach, KF (1979) Simultaneous and successive color contrast expressed in ‘slow’ phototactic behavior of walking Drosophila melanogaster. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 130, 161–171.Google Scholar
Goulson, D (1997) Wipfelkrankheit: modification of host behavior during baculoviral infection. Oecologia 109, 219–228.CrossRefGoogle ScholarPubMed
Han, Y, van Houte, S, Drees, GF, van Oers, MM and Ros, VID (2015) Parasitic manipulation of host behavior: baculovirus SeMNPV EGT facilitates tree-top disease in Spodoptera exigua larvae by extending the time to death. Insects 6, 716–731.Google Scholar
Hoover, K, Grove, M, Gardner, M, Hughes, DP, McNeil, J and Slavicek, J (2011) A gene for an extended phenotype. Science 333, 1401.Google Scholar
Hughes, D (2013) Pathways to understanding the extended phenotype of parasites in their hosts. Journal of Experimental Biology 216, 142–147.CrossRefGoogle ScholarPubMed
Kamita, SG, Nagasaka, K, Chua, JW, Shimada, T, Mita, K, Kobayashi, M, Maeda, S and Hammock, BD (2005) A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proceedings of the National Academy of Sciences of the United States of America 102, 2584–2589.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
Keene, AC and Sprecher, SG (2012) Seeing the light: photobehavior in fruit fly larvae. Trends in Neurosciences 35, 104–110.Google Scholar
Lefèvre, T, Adamo, SA, Biron, DG, Misse, D, Hughes, D and Thomas, F (2009) Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Advances in Parasitology 68, 45–83.Google Scholar
Libersat, F, Delago, A and Gal, R (2009) Manipulation of host behavir by parasitic insects and insect parasites. Annual Review of Entomology 54, 189–207.Google Scholar
Murillo, R, Elvira, S, Muñoz, D, Williams, T and Caballero, P (2006) Genetic and phenotypic variability in Spodoptera exigua nucleopolyhedrovirus isolates from greenhouse soils in southern Spain. Biological Control 38, 157–165.Google Scholar
Otsuna, H, Shinomiya, K and Ito, K (2014) Parallel neural pathways in higher visual centers of the Drosophila brain that mediate wavelength-specific behavior. Frontiers in Neural Circuits 8, 1–8.Google Scholar
Ponton, F, Lefèvre, T, Lebarbenchon, C, Thomas, F, Loxdale, HD, Marché, L, Renault, L, Perrot-Minnot, MJ and Biron, DG (2006) Do distantly related parasites rely on the same proximate factors to alter the behavior of their hosts? Proceedings of the Royal Society of London B: Biological Sciences 273, 2869–2877.Google Scholar
Ponton, F, Otálora-Luna, F, Lefèvre, T, Guerin, PM, Lebarbenchon, C, Duneau, D, Biron, DG and Thomas, F (2011) Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation. Behaviour Ecology 22, 392–400.Google Scholar
R Core Team (2013) A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.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
Smits, PH, van de Vrie, M and Vlak, JM (1986) Oviposition of beet armyworm (Lepidoptera: Noctuidae) on greenhouse crops. Environmental Entomology 15, 1189–1191.Google Scholar
Sun, YX, Tian, A, Zhang, XB, Zhao, ZG, Zhang, ZW and Ma, RY (2014) Phototaxis of Grapholitha molesta (Lepidoptera: Olethreutidae) to different light sources. Journal of Economic Entomology 107, 1792–1799.Google Scholar
Tain, L, Perrot-Minnot, MJ and Cézilly, F (2006) Altered host behavior and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proceedings of the Royal Society of London B: Biological Sciences 273, 3039–3045.Google Scholar
van Houte, S, Ros, VID, Mastenbroek, TG, Vendrig, NJ, Hoover, K, Spitzen, J and van Oers, MM (2012) Protein tyrosine phosphatase-induced hyperactivity is a conserved strategy of a subset of baculoviruses to manipulate lepidopteran host behavior. PLoS ONE 7, e46933.Google Scholar
van Houte, S, Ros, VID and van Oers, MM (2013) Walking with insects: molecular mechanisms behind parasitic manipulation of host behavior. Molecular Ecology 22, 3458–3475.Google Scholar
van Houte, S, van Oers, MM, Han, Y, Vlak, JM and Ros, VID (2014) Baculovirus infection triggers a positive phototactic response in caterpillars to induce ‘tree-top’ disease. Biology Letters 10, 20140680.Google Scholar
van Houte, S, van Oers, MM, Han, Y, Vlak, JM and Ros, VID (2015) Baculovirus infection triggers a positive phototactic response in caterpillars: a response to Dobson et al. (2015) Biology Letters 11, 20150633.Google Scholar
Wesołowska, W and Wesołowski, T (2014) Do Leucochloridium sporocysts manipulate the behavior of their snail hosts? Journal of Zoology 292, 151–155.Google Scholar
Williams, T, Bergoin, M and van Oers, MM (2017) Diversity of large DNA viruses of invertebrates. Journal of Invertebrate Pathology 147, 4–22.Google Scholar
Yamaguchi, S and Heisenberg, M (2011) Photoreceptors and neural circuitry underlying phototaxis in insects. Fly 5, 333–336.Google Scholar
Supplementary material: PDF

Han et al supplementary material

Han et al supplementary material 1

Download Han et al supplementary material(PDF)
PDF 336.7 KB