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Virus-Induced Behavioural Changes in Insects

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Host Manipulations by Parasites and Viruses

Part of the book series: Parasitology Research Monographs ((Parasitology Res. Monogr.,volume 7))

Abstract

Increasing evidence shows that host behaviour often changes following infection by a variety of parasites, including viruses. The altered behaviour is either induced by the parasites to enhance parasite survival and transmission, or is a response of the host to avoid spread of infection in the host population. Given the high prevalence of viruses among insects, in a virus-host interaction or in a virus-vector relationship, viruses might have a huge impact on insect behaviour. This review first describes known examples of changes in insect behaviour upon virus infection. Although scarce, any known information on the underlying mechanism is also included. Special attention is given to baculoviruses and the hyperactivity and tree-top disease that they induce in their caterpillar hosts, so far the best studied systems in this research field. Subsequently, we discuss the virus-induced changes in insect behaviour from an ecological and evolutionary point of view.

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References

  • Adamo SA (2008) Bidirectional connections between the immune system and the nervous system in insects. In: Beckage NE (ed) Insect immunology. Academic, San Diego, pp 129–149

    Chapter  Google Scholar 

  • Adamo SA (2014) Parasitic aphrodisiacs: manipulation of the hosts’ behavioral defenses by sexually transmitted parasites. Integr Comp Biol 54:159–165

    Article  CAS  PubMed  Google Scholar 

  • Adamo SA, Bartlett A, Le J, Spencer N, Sullivan K (2010) Illness-induced anorexia may reduce trade-offs between digestion and immune function. Anim Behav 79:3–10

    Article  Google Scholar 

  • Adamo SA, Kovalko I, Easy RH, Stoltz D (2014) A viral aphrodisiac in the cricket Gryllus texensis. J Exp Biol 217:1970–1976

    Article  PubMed  Google Scholar 

  • Ball BV (1989) Varroa jacobsoni as a virus vector. In: Cavalloro R (ed) Present status of varroatosis in Europe and progress in the Varroa mite control. Office Official Publications EC, Luxembourg, pp 241–244

    Google Scholar 

  • Ban L, Ahmed E, Ninkovic V, Delp G, Glinwood R (2008) Infection with an insect virus affects olfactory behaviour and interactions with host plant and natural enemies in an aphid. Entomol Exp Appl 127:108–117

    Article  Google Scholar 

  • Baracchi D, Fadda A, Turillazzi S (2012) Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J Insect Physiol 58:1589–1596

    Article  CAS  PubMed  Google Scholar 

  • Bennett KE, Hopper JE, Stuart MA, West M, Drolet BS (2008) Blood-feeding behavior of vesicular stomatitis virus infected Culicoides sonorensis (Diptera: Ceratopogonidae). J Med Entomol 45:921–926

    Article  PubMed  Google Scholar 

  • Burand JP (2009) The sexually transmitted insect virus, Hz-2 V. Virol Sin 24:428–435

    Article  Google Scholar 

  • Burand JP, Tan W (2006) Mate preference and mating behavior of male Helicoverpa zea (Lepidoptera: Noctuidae) infected with the sexually transmitted insect virus Hz-2 V. Ann Entomol Soc Am 99:969–973

    Article  Google Scholar 

  • Burand JP, Rallis CP, Tan W (2004) Horizontal transmission of Hz-2 V by virus infected Helicoverpa zea moths. J Invertebr Pathol 85:128–131

    Article  PubMed  Google Scholar 

  • Burand JP, Tan W, Kim W, Nojima S, Roelofs W (2005) Infection with the insect virus Hz-2v alters mating behavior and pheromone production in female Helicoverpa zea moths. J Insect Sci 5:1–6

    Article  Google Scholar 

  • Cézilly F, Thomas F, Médoc V, Perrot-Minnot M-J (2010) Host-manipulation by parasites with complex life cycles: adaptive or not? Trends Parasitol 26:311–317

    Article  PubMed  Google Scholar 

  • Chapman AD (2006) Numbers of living species in Australia and the World. Australian Biological Resources Study, Canberra

    Google Scholar 

  • Cory JS, Hoover K (2006) Plant-mediated effects in insect-pathogen interactions. Trends Ecol Evol 21:278–286

    Article  PubMed  Google Scholar 

  • Cranston PS (2010) Insect biodiversity and conservation in Australasia. Annu Rev Entomol 55:55–75

    Article  CAS  PubMed  Google Scholar 

  • Dawkins RL (1982) The extended phenotype. Oxford University Press, Oxford

    Google Scholar 

  • de Bekker C, Merrow M, Hughes DP (2014) From behavior to mechanisms: an integrative approach to the manipulation by a parasitic fungus (Ophiocordyceps unilateralis s.l.) of its host ants (Camponotus spp.). Integr Comp Biol 54:166–176

    Article  PubMed  Google Scholar 

  • Dheilly NM, Maure F, Ravallec M, Galinier R, Doyon J, Duval D, Leger L, Volkoff AN, Misse D, Nidelet S, Demolombe V, Brodeur J, Gourbal B, Thomas F, Mitta G (2015) Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proc R Soc B 282:20142773

    Article  PubMed  Google Scholar 

  • Entwistle PF, Forkner AC, Green BM, Cory JS (1993) Avian dispersal of nuclear polyhedrosis viruses after induced epizootics in the pine beauty moth, Panolis flammea (Lepidoptera: Noctuidae). Bio Control 3:61–69

    Article  Google Scholar 

  • Evans HF, Allaway GP (1983) Dynamics of baculovirus growth and dispersal in Mamestra brassicae L. (Lepidoptera: Noctuidae) larval populations introduced into small cabbage plots. Appl Environ Microbiol 45:493–501

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fedorka KM, Mousseau TA (2007) Immune system activation affects male sexual signal and reproductive potential in crickets. Behav Ecol 18:231–235

    Article  Google Scholar 

  • Fereres A, Shukle RH, Araya JE, Foster JE (1990) Probing and feeding behavior of Sitobion avenae (F.) (Horn., Aphididae) on three wheat cultivars infected with barley yellow dwarf virus. J Appl Entomol 109:29–36

    Article  Google Scholar 

  • Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T, Nomoto A, Kubo T (2004) Novel insect Picorna-like virus identified in the brains of aggressive worker honeybees. J Virol 78:1093–1100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T, Nomoto A, Kubo T (2005) Kakugo virus from brains of aggressive worker honeybees. Adv Virus Res 65:1–27

    Article  CAS  PubMed  Google Scholar 

  • Gabitzsch ES, Blair CD, Beaty BJ (2006) Effect of La Crosse Virus infection on insemination rates in female Aedes triseriatus (Diptera: Culicidae). J Med Entomol 43:850–852

    Article  CAS  PubMed  Google Scholar 

  • Gandon S, Rivero A, Varaldi J (2006) Superparasitism evolution: adaptation or manipulation? Am Nat 167:1–22

    Article  Google Scholar 

  • Gisder S, Aumeier P, Genersch E (2009) Deformed wing virus: replication and viral load in mites (Varroa destructor). J Gen Virol 90:463–467

    Article  CAS  PubMed  Google Scholar 

  • Goulson D (1997) Wipfelkrankheit: modification of host behaviour during baculoviral infection. Oecologia 109:219–228

    Article  Google Scholar 

  • Grimstad PR, Ross QE, Craig GB Jr (1980) Aedes triseriatus (Diptera: Culicidae) and La Crosse virus. II. Modification of mosquito feeding behavior by virus infection. J Med Entomol 17:1–7

    Article  CAS  PubMed  Google Scholar 

  • Hamblin S, Tanaka M (2013) Behavioural manipulation of insect hosts by Baculoviridae as a process of niche construction. BMC Evol Biol 13:170

    Article  PubMed Central  PubMed  Google Scholar 

  • Hamm JJ, Carpenter JE, Styer EL (1996) Oviposition day effect on incidence of agonadal progeny of Helicoverpa zea (Lepidoptera: Noctuidae) infected with a virus. Ann Entomol Soc Am 89:266–275

    Article  Google Scholar 

  • Harris JW (2007) Bees with Varroa Sensitive Hygiene preferentially remove mite infested pupae aged ≤ five days post capping. J Apicult Res 46:134–139

    Article  Google Scholar 

  • Hofmann O (1891) Insektentötende Pilze mit bosenderer Berücksichtigung der Nonne. P. Weber, Frankfurt

    Google Scholar 

  • Hoover K, Grove M, Gardner M, Hughes DP, McNeil J, Slavicek J (2011) A gene for an extended phenotype. Science 333:1401

    Article  CAS  PubMed  Google Scholar 

  • Hu Z, Zhao H, Thieme T (2013) Modification of non-vector aphid feeding behavior on virus-infected host plant. J Insect Sci 13:1–11

    Article  Google Scholar 

  • Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecol 11:173

    Article  Google Scholar 

  • Ingwell LL, Eigenbrode SD, Bosque-Perez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578

    Article  PubMed Central  PubMed  Google Scholar 

  • Iqbal J, Mueller U (2007) Virus infection causes specific learning deficits in honeybee foragers. Proc R Soc B 274:1517–1521

    Article  PubMed Central  PubMed  Google Scholar 

  • Jackson BT, Brewster CC, Paulson SL (2012) La Crosse virus infection alters blood feeding behavior in Aedes triseriatus and Aedes albopictus (Diptera: Culicidae). J Med Entomol 49:1424–1429

    Article  PubMed Central  PubMed  Google Scholar 

  • Jacot A, Scheuber H, Brinkhof MW (2004) Costs of an induced immune response on sexual display and longevity in field crickets. Evolution 58:2280–2286

    Article  PubMed  Google Scholar 

  • Jakob NJ, Kleespies RG, Tidona CA, Müller K, Gelderblom HR, Darai G (2002) Comparative analysis of the genome and host range characteristics of two insect iridoviruses: Chilo iridescent virus and a cricket iridovirus isolate. J Gen Virol 83:463–470

    Article  CAS  PubMed  Google Scholar 

  • Jenkins DA, Hunter WB, Goenaga R (2011) Effects of invertebrate iridescent virus 6 in Phyllophaga vandinei and its potential as a biocontrol delivery system. J Insect Sci 11:44

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kamita SG, Nagasaka K, Chua JW, Shimada T, Mita K, Kobayashi M, Maeda S, Hammock BD (2005) A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci U S A 102:2584–2589

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Katsuma S, Koyano Y, Kang W, Kokusho R, Kamita S, Shimada T (2012) The baculovirus uses a captured host phosphatase to induce enhanced locomotory activity in host caterpillars. PLoS Pathog 8:e1002644

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kleespies RG, Tidona CA, Darai G (1999) Characterization of a new iridovirus isolated from crickets and investigations on the host range. J Invertebr Pathol 73:84–90

    Article  PubMed  Google Scholar 

  • Kulinčević JM, Stairs GR, Rothenbuhler WC (1969) A disease of the honey bee causing behavioral changes and mortality. J Invertebr Pathol 14:13–17

    Article  PubMed  Google Scholar 

  • Lafferty KD, Kruis AM (2012) Ecological consequences of manipulative parasites. In: Hughes DP, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford University Press, Oxford, pp 158–171

    Chapter  Google Scholar 

  • Lawniczak MKN, Barnes AI, Linklater JR, Boone JM, Wigby S, Chapman T (2007) Mating and immunity in invertebrates. Trends Ecol Evol 22:48–55

    Article  PubMed  Google Scholar 

  • Lee JH, Rowley WA, Platt KB (2000) Longevity and spontaneous flight activity of Culex tarsalis (Diptera: Culicidae) infected with western equine encephalomyelitis virus. J Med Entomol 37:187–193

    Article  CAS  PubMed  Google Scholar 

  • Lefèvre T, Thomas F (2008) Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect Genet Evol 8:504–519

    Article  PubMed  Google Scholar 

  • Lefèvre T, Adamo S, Biron D, Misse D, Hughes D, Thomas F (2009) Invasion of the body snatchers: the diversity and evolution of manipulation strategies in host-parasite interactions. Adv Parasitol 68:45–83

    Article  PubMed  Google Scholar 

  • Leman JC, Weddle CB, Gershman SN, Kerr AM, Ower GD, St John JM, Vogel LA, Sakaluk SK (2009) Lovesick: immunological costs of mating to male sagebrush crickets. J Evol Biol 22:163–171

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Chen Y, Zhang S, Chen S, Li W, Yan L, Shi L, Wu L, Sohr A, Su S (2013) Viral infection affects sucrose responsiveness and moming ability of forager honey bees, Apis mellifera L. PLoS One 8:e77354

    Google Scholar 

  • Lima-Camara TN, Bruno RV, Luz PM, Castro MG, Lourenco-de-Oliveira R, Sorgine MH, Peixoto AA (2011) Dengue infection increases the locomotor activity of Aedes aegypti females. PLoS One 6:0017690

    Article  Google Scholar 

  • Martinez J, Duplouy A, Woolfit M, Vavre F, O’Neill SL, Varaldi J (2012) Influence of the virus LbFV and of Wolbachia in a host-parasitoid interaction. PLoS One 7:e35081

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mauck K, Bosque-Pérez NA, Eigenbrode SD, de Moraes CM, Mescher MC (2012) Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses. Funct Ecol 26:1162–1175

    Article  Google Scholar 

  • Maure F, Daoust SP, Brodeur J, Mitta G, Thomas F (2013) Diversity and evolution of bodyguard manipulation. J Exp Biol 216(1):36–42

    Article  PubMed  Google Scholar 

  • Medina-Ortega KJ, Bosque-Perez NA, Ngumbi E, Jimenez-Martinez ES, Eigenbrode SD (2009) Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from Barley yellow dwarf virus-infected wheat. Environ Entomol 38:836–845

    Article  CAS  PubMed  Google Scholar 

  • Miller LK, Ball LA (1998) The insect viruses. Plenum Press, New York

    Book  Google Scholar 

  • Moreno-Delafuente A, Garzo E, Moreno A, Fereres A (2013) A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLoS One 8:e61543

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nalçacıoğlu R, Ince I, Demirbağ Z (2009) The biology of Chilo iridescent virus. Virol Sin 24:285–294

    Article  Google Scholar 

  • Patot S, Lepetit D, Charif D, Varaldi J, Fleury F (2009) Molecular detection, penetrance, and transmission of an inherited virus responsible for behavioral manipulation of an insect parasitoid. Appl Environ Microbiol 75:703–710

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Patot S, Martinez J, Allemand R, Gandon S, Varaldi J, Fleury F (2010) Prevalence of a virus inducing behavioural manipulation near species range border. Mol Ecol 19:2995–3007

    Article  CAS  PubMed  Google Scholar 

  • Platt K, Linthicum K, Myint K, Innis B, Lerdthusnee K, Vaughn D (1997) Impact of dengue virus infection on feeding behavior of Aedes aegypti. Am J Trop Med Hygiene 57:119–125

    CAS  Google Scholar 

  • Ponton F, Lefèvre T, Lebarbenchon C, Thomas F, Loxdale HD, Marché L, Renault L, Perrot-Minnot MJ, Biron DG (2006) Do distantly related parasites rely on the same proximate factors to alter the behaviour of their hosts? Proc R Soc B 273:2869–2877

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Putnam JL, Scott TW (1995) Blood-feeding behavior of dengue-2 virus-infected Aedes aegypti. Am J Trop Med Hyg 52:225–227

    CAS  PubMed  Google Scholar 

  • Qualls WA, Day JF, Xue RD, Bowers DF (2012) Sindbis virus infection alters blood feeding responses and DEET repellency in Aedes aegypti (Diptera: Culicidae). J Med Entomol 49:418–423

    Article  CAS  PubMed  Google Scholar 

  • Raina AK, Adams JR (1995) Gonad-specific virus of corn earworm. Nature 374:770

    Article  CAS  Google Scholar 

  • Raina AK, Kingan TG, Giebltowicz JM (1994) Mating-induced loss of sex pheromone and sexual receptivity in insects with emphasis on Helicoverpa zea and Lymantria dispar. Arch Insect Biochem Physiol 25:317–327

    Article  CAS  Google Scholar 

  • Rajabaskar D, Bosque-Pérez NA, Eigenbrode SD (2014) Preference by a virus vector for infected plants is reversed after virus acquisition. Virus Res 186:32–37

    Article  CAS  PubMed  Google Scholar 

  • Raymond B, Hartley SE, Cory JS, Hails RS (2005) The role of food plant and pathogen-induced behaviour in the persistence of a nucleopolyhedrovirus. J Invertebr Pathol 88:49–57

    Article  PubMed  Google Scholar 

  • Reese SM, Beaty MK, Gabitzsch ES, Blair CD, Beaty BJ (2009) Aedes triseriatus females transovarially infected with La Crosse virus mate more efficiently than uninfected mosquitoes. J Med Entomol 46:1152–1158

    Article  PubMed Central  PubMed  Google Scholar 

  • Richard FJ, Aubert A, Grozinger CM (2008) Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 6:50

    Article  PubMed Central  PubMed  Google Scholar 

  • Richard FJ, Holt HL, Grozinger CM (2012) Effects of immunostimulation on social behaviour, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics 13:558

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rortais A, Tentcheva D, Papachristoforou A, Gauthier L, Arnold G, Colin ME, Bergoin M (2006) Deformed wing virus is not related to honey bees’ aggressiveness. Virol J 3:61

    Article  PubMed Central  PubMed  Google Scholar 

  • Ros VID, van Houte S, Hemerik L, van Oers MM (2015) Baculovirus-induced tree-top disease: how extended is the role of egt as a gene for the extended phenotype? Mol Ecol 24:249–258

    Google Scholar 

  • Salvy M, Martin C, Bagnères AG, Provost É, Roux M, Le Conte Y, Clément JL (2001) Modifications of the cuticular hydrocarbon profile of Apis mellifera worker bees in the presence of the ectoparasitic mite Varroa jacobsoni in brood cells. Parasitology 122:145–159

    Article  CAS  PubMed  Google Scholar 

  • Sato T, Watanabe K, Kanaiwa M, Niizuma Y, Harada Y, Lafferty KD (2011) Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92:201–207

    Article  PubMed  Google Scholar 

  • Schöning C, Gisder S, Geiselhardt S, Kretschmann I, Bienefeld K, Hilker M, Genersch E (2012) Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera. J Exp Biol 215:264–271

    Article  PubMed  Google Scholar 

  • Shah KS, Evans EC, Pizzorno MC (2009) Localization of deformed wing virus (DWV) in the brains of the honeybee, Apis mellifera Linnaeus. Virol J 6:182

    Article  PubMed Central  PubMed  Google Scholar 

  • Smirnoff WA (1965) Observations on the effect of virus infection on insect behavior. J Invertebr Pathol 7:387–388

    Article  CAS  PubMed  Google Scholar 

  • Stafford CA, Walker GP, Ullman DE (2011) Infection with a plant virus modifies vector feeding behavior. Proc Natl Acad Sci U S A 108:9350–9355

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sumpter DJT, Martin SJ (2004) The dynamics of virus epidemics in Varroa-infested honey bee colonies. J Anim Ecol 73:51–63

    Article  Google Scholar 

  • Thomas F, Schmidt-Rhaesa A, Martin G, Manu C, Durand P, Renaud F (2002) Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? J Evol Biol 15:356–361

    Article  Google Scholar 

  • Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Processes 68:185–199

    Article  PubMed  Google Scholar 

  • Turell MJ, Gargan TP, Bailey CL (1985) Culex pipiens (Diptera: Culicidae) morbidity and mortality associated with Rift Valley fever virus infection. J Med Entomol 22:332–337

    Article  CAS  PubMed  Google Scholar 

  • van Alphen JJ, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu Rev Entomol 351:59–79

    Article  Google Scholar 

  • van de Wetering F, Hulshof J, Posthuma K, Harrewijn P, Goldbach R, Peters D (1998) Distinct feeding behavior between sexes of Frankliniella occidentalis results in higher scar production and lower tospovirus transmission by females. Entomol Exp Appl 88:9–15

    Article  Google Scholar 

  • van Houte S, Ros VID, Mastenbroek TG, Vendrig NJ, Hoover K, Spitzen J, 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

    Article  PubMed Central  PubMed  Google Scholar 

  • van Houte S, Ros VID, van Oers MM (2013) Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. Mol Ecol 22:3458–3475

    Article  PubMed  Google Scholar 

  • van Houte S, Ros VID, van Oers MM (2014a) Hyperactivity and tree-top disease induced by the baculovirus AcMNPV in Spodoptera exigua larvae are governed by independent mechanisms. Naturwissenschaften 101:347–350

    Article  PubMed  Google Scholar 

  • van Houte S, van Oers MM, Han Y, Vlak JM, Ros VID (2014b) Baculovirus infection triggers a positive phototactic response in caterpillars to induce ‘tree-top’ disease. Biol Lett 10:20140680

    Article  PubMed  Google Scholar 

  • Varaldi J, Fouillet P, Ravallec M, Lopez-Ferber M, Bouletreau M, Fleury F (2003) Infectious behaviour in a parasitoid. Science 302:1930

    Article  CAS  PubMed  Google Scholar 

  • Varaldi J, Bouletreau M, Fleury F (2005) Cost induced by viral particles manipulating superparasitism behaviour in the parasitoid Leptopilina boulardi. Parasitology 131:161–168

    Article  CAS  PubMed  Google Scholar 

  • Varaldi J, Petit S, Bouletreau M, Fleury F (2006) The virus infecting the parasitoid Leptopilina boulardi exerts a specific action on superparasitism behaviour. Parasitology 132:747–756

    Article  CAS  PubMed  Google Scholar 

  • Varaldi J, Patot S, Nardin M, Gandon S (2009) A virus-shaping reproductive strategy in a Drosophila parasitoid. Adv Parasitol 70:333–363

    Article  PubMed  Google Scholar 

  • Varaldi J, Martinez J, Patot S, Lepetit D, Fleury F, Gandon S, Drezen JM, Beckage NE (2012) An inherited virus manipulating the behaviour of its parasitoid host: epidemiology and evolutionary consequences. In: Beckage NE, Drezen JM (eds) Parasitoid viruses: symbionts and pathogens. Academic, San Diego, pp 203–214

    Chapter  Google Scholar 

  • Vasconcelos SD, Cory JS, Wilson KR, Sait SM, Hails RS (1996) Modified behaviour in baculovirus-infected lepidopteran larvae and its impact on the spatial distribution of inoculum. Bio Contr 7:299–306

    Article  Google Scholar 

  • Williamson C, Rybicki EP, Kasdorf GGF, Von Wechmar MB (1988) Characterization of a new picorna-like virus isolated from aphids. J Gen Virol 69:787–795

    Article  CAS  Google Scholar 

  • Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Cox-Foster DL (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci U S A 102:7470–7475

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Kelli Hoover for critically reading the manuscript, for useful suggestions and for sharing unpublished data. René van der Vlugt is acknowledged for careful reading of several sections prior to submission. Vera I.D. Ros was financed by a VENI-grant from the Netherlands Organisation for Scientific Research (project 863.11.017).

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Authors and Affiliations

  1. Laboratory of Virology, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands

    Yue Han, Monique M. van Oers, Stineke van Houte & Vera I. D. Ros

  2. Department of Biosciences, Centre for Ecology and Conservation, University of Exeter, Penryn, Cornwall, UK

    Stineke van Houte

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  1. Yue Han
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  2. Monique M. van Oers
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  4. Vera I. D. Ros
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Correspondence to Monique M. van Oers .

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  1. Department of Zoomorphology, Cell Biology and Parasitology, Heinrich Heine University, Universitätsstrasse 1, Düsseldorf, Germany

    Heinz Mehlhorn

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Han, Y., van Oers, M.M., van Houte, S., Ros, V.I.D. (2015). Virus-Induced Behavioural Changes in Insects. In: Mehlhorn, H. (eds) Host Manipulations by Parasites and Viruses. Parasitology Research Monographs, vol 7. Springer, Cham. https://doi.org/10.1007/978-3-319-22936-2_10

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