1932

Abstract

Insect behavior can be manipulated by parasites, and in many cases, such manipulation involves the central and peripheral nervous system. Neuroparasitology is an emerging branch of biology that deals with parasites that can control the nervous system of their host. The diversity of parasites that can manipulate insect behavior ranges from viruses to macroscopic worms and also includes other insects that have evolved to become parasites (notably, parasitic wasps). It is remarkable that the precise manipulation observed does not require direct entry into the insect brain and can even occur when the parasite is outside the body. We suggest that a spatial view of manipulation provides a holistic approach to examining such interactions. Integration across approaches from natural history to advanced imaging techniques, omics, and experiments will provide new vistas in neuroparasitology. We also suggest that for researchers interested in the proximate mechanisms of insect behaviors, studies of parasites that have evolved to control such behavior is of significant value.

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2018-01-07
2024-04-20
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Literature Cited

  1. Adamo SA. 1.  2012. The strings of the puppet master: how parasites change host behavior. See Ref. 32 36–51
  2. Adamo SA, Easy RH, Kovalko I, MacDonald J, McKeen A. 2.  et al. 2017. Predator exposure-induced immunosuppression: trade-off, immune redistribution or immune reconfiguration?. J. Exp. Biol. 220:868–75 [Google Scholar]
  3. Adamo SA, Webster JP. 3.  2013. Neural parasitology: how parasites manipulate host behaviour. J. Exp. Biol. 216:1–2 [Google Scholar]
  4. Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL. 4.  et al. 2009. The life of a dead ant: the expression of an adaptive extended phenotype. Am. Nat. 174:424–33 [Google Scholar]
  5. Artiushin G, Sehgal A. 5.  2017. The Drosophila circuitry of sleep–wake regulation. Curr. Opin. Neurobiol. 44:243–50 [Google Scholar]
  6. Askew RR. 6.  1971. Parasitic Insects New York: Heinemann Educ. Publ. Inc.
  7. Beckage NE, Gelman DB. 7.  2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49:299–330 [Google Scholar]
  8. Biron DG, Ponton F, Marche L, Galeotti N, Renault L. 8.  et al. 2006. ‘Suicide’ of crickets harbouring hairworms: a proteomics investigation. Insect Mol. Biol. 15:731–42 [Google Scholar]
  9. Bohart RM. 9.  1941. A revision of the Strepsiptera with special reference to the species of North America. Univ. Calif. Publ. Entomol. 7:91–160 [Google Scholar]
  10. Carney WP. 10.  1969. Behavioral and morphological changes in carpenter ants harboring Dicrocoeliid metacercariae. Am. Midland Nat. 82:605–11 [Google Scholar]
  11. Carney WP. 11.  1970. Brachylecithum mosquensis: infections in vertebrate, molluscan and arthropod hosts. Trans. Am. Microsc. Soc. 89:233–50 [Google Scholar]
  12. Dawkins R. 12.  2012. Foreword. See Ref. 32 xi–xiii
  13. Dheilly NM, Maure F, Ravallec M, Galinier R, Doyon J. 13.  et al. 2015. Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proc. R. Soc. Lond. B. 282:20142773 [Google Scholar]
  14. Eberhard WG. 14.  2000. Spider manipulation by a wasp larva. Nature 406:255–56 [Google Scholar]
  15. Emanuel S, Libersat F. 15.  2017. Do quiescence and wasp venom-induced lethargy share common neuronal mechanisms in cockroaches?. PLOS ONE 12:e0168032 [Google Scholar]
  16. Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T. 16.  et al. 2004. Novel insect picorna-like virus identified in the brains of aggressive worker honeybees. J. Virol. 78:1093–100 [Google Scholar]
  17. Gal R, Kaiser M, Haspel G, Libersat F. 17.  2014. Sensory arsenal on the stinger of the parasitoid jewel wasp and its possible role in identifying cockroach brains. PLOS ONE 9:e89683 [Google Scholar]
  18. Gal R, Libersat F. 18.  2008. A parasitoid wasp manipulates the drive for walking of its cockroach prey. Curr Biol 18:877–82 [Google Scholar]
  19. Gavra T, Libersat F. 19.  2011. Involvement of the opioid system in the hypokinetic state induced in cockroaches by a parasitoid wasp. J. Comp. Physiol. 197:279–91 [Google Scholar]
  20. Geffre AC, Liu R, Manfredini F, Beani L, Kathirithamby J. 20.  et al. 2017. Transcriptomics of an extended phenotype: parasite manipulation of wasp social behaviour shifts expression of caste-related genes. Proc. R. Soc. B 284:20170029 [Google Scholar]
  21. Godfray HCJ. 21.  1994. Parasitoids Princeton, NJ: Princeton Univ. Press
  22. Grosman AH, Janssen EF, de Brito EG, Cordeiro F, Colares JO. 22.  et al. 2008. Parasitoid increases survival of its pupae by inducing hosts to fight predators. PLOS ONE 3:6e2276 [Google Scholar]
  23. Han Y, van Oers MM, van Houte S, Ros VI. 23.  2015. Virus-induced behavioural changes in insects. Host Manipulations by Parasites and Viruses H. Mehlhorn 149–74 Cham: Springer Int. Switz. [Google Scholar]
  24. Haspel G, Rosenberg LA, Libersat F. 24.  2003. Direct injection of venom by a predatory wasp into cockroach brain. J. Neurobiol. 56:287–92 [Google Scholar]
  25. Hojo MK, Pierce NE, Tsuji K. 25.  2015. Lycaenid caterpillar secretions manipulate attendant ant behavior. Curr. Biol. 25:2260–64 [Google Scholar]
  26. Hoover K, Grove M, Gardner M, Hughes DP, McNeil J, Slavicek J. 26.  2011. A gene for an extended phenotype. Science 333:1401 [Google Scholar]
  27. Hughes AL. 27.  2013. Origin of ecdysosteroid UDP-glycosyltransferases of baculoviruses through horizontal gene transfer from Lepidoptera. Coevolution 1:1–7 [Google Scholar]
  28. Hughes DP. 28.  2014. On the origins of parasite extended phenotypes. Integr. Comp. Biol. 54:210–7 [Google Scholar]
  29. Hughes DP. 29.  2015. Behavioral ecology: manipulative mutualism. Curr. Biol. 25:R806–8 [Google Scholar]
  30. Hughes DP, Andersen S, Hywel-Jones NL, Himaman W, Bilen J, Boomsma JJ. 30.  2011. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecol 11:3 [Google Scholar]
  31. Hughes DP, Araujo J, Loreto RG, Quevillon L, de Bekker C, Evans HC. 31.  2016. From so simple a beginning: the evolution of behavioral manipulation by fungi. Adv. Genet. 94:437–69 [Google Scholar]
  32. Hughes DP, Brodeur J, Thomas F. 32. , eds. 2012. Host Manipulation by Parasites Oxford, UK: Oxord Univ. Press
  33. Hughes DP, Kathirithamby J. 33.  2005. Cost of strepsipteran macroparasitism for immature wasps: Does sociality modulate virulence?. Oikos 110:428–34 [Google Scholar]
  34. Hughes DP, Kathirithamby J, Turillazzi S, Beani L. 34.  2004. Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation?. Behav. Ecol. 15:1037–43 [Google Scholar]
  35. Hughes DP, Moya-Raygoza G, Kathirithamby J. 35.  2003. The first record among Dolichoderinae (Formicidae) of parasitism by Strepsiptera. Insectes Sociaux 50:148–50 [Google Scholar]
  36. Kaiser M, Libersat F. 36.  2015. The role of the cerebral ganglia in the venom-induced behavioral manipulation of cockroaches stung by the parasitoid jewel wasp. J. Exp. Biol. 218:1022–27 [Google Scholar]
  37. Kloss TG, Gonzaga MO, de Oliveira LL, Sperber CF. 37.  2017. Proximate mechanism of behavioral manipulation of an orb-weaver spider host by a parasitoid wasp. PLOS ONE 12:e0171336 [Google Scholar]
  38. Kloss TG, Gonzaga MO, Roxinol JAM, Sperber CF. 38.  2016. Attack behavior of two wasp species of the Polysphincta genus group (Hymenoptera, Ichneumonidae) on their orb-weaver spider hosts (Araneae, Araneidae). J. Insect Behav. 29:315–24 [Google Scholar]
  39. Konno K, Kazuma K, Nihei K-i. 39.  2016. Peptide toxins in solitary wasp venoms. Toxins 8:114 [Google Scholar]
  40. Korenko S, Pekár S. 40.  2011. A parasitoid wasp induces overwintering behaviour in its spider host. PLOS ONE 6:e24628 [Google Scholar]
  41. Lach L, Parr CL, Abboutt KL. 41. , eds. 2010. Ant Ecology Oxford, UK: Oxford Univ. Press
  42. Libersat F, Gal R. 42.  2014. Wasp voodoo rituals, venom-cocktails, and the zombification of cockroach hosts. Integr. Comp. Biol. 54:129–42 [Google Scholar]
  43. Libersat F, Pflueger H-J. 43.  2004. Monoamines and the orchestration of behavior. BioScience 54:17–25 [Google Scholar]
  44. Loreto RG, Elliot SL, Freitas ML, Pereira TM, Hughes DP. 44.  2014. Long-term disease dynamics for a specialized parasite of ant societies: a field study. PLOS ONEe103516
  45. Lucius R, Romig T, Frank W. 45.  1980. Camponotus compressiscapus André (Hymenoptera, Formicidae) an experimental second intermediate host of Dicrocoelium hospes looss, 1907 (Trematodes, Dicrocoeliidae). Parasitol. Res. 63:271–75 [Google Scholar]
  46. Maeyama T, Terayama M, Matsumoto T. 46.  1994. The abnormal behavior of Colobopsis sp. (Hymenoptera: Formicidae) parasitized by Mermis (Nematoda) in Papua New Guinea. Sociobiology 24:115–19 [Google Scholar]
  47. Maure F, Daoust SP, Brodeur J, Mitta G, Thomas F. 47.  2013. Diversity and evolution of bodyguard manipulation. J. Exp. Biol. 216:36–42 [Google Scholar]
  48. Miles CI, Booker R. 48.  2000. Octopamine mimics the effects of parasitism on the foregut of the tobacco hornworm Manduca sexta. J. Exp. Biol. 203:1689–700 [Google Scholar]
  49. Möbius P, Penzlin H. 49.  1993. Stress-induced release of octopamine in the American cockroach Periplaneta americana L. Acta Biol. Hung. 44:45–50 [Google Scholar]
  50. Moore EL, Haspel G, Libersat F, Adams ME. 50.  2006. Parasitoid wasp sting: a cocktail of GABA, taurine, and β‐alanine opens chloride channels for central synaptic block and transient paralysis of a cockroach host. J. Neurobiol. 66:811–20 [Google Scholar]
  51. Moore J. 51.  2002. Parasites and the Behavior of Animals Oxford, UK: Oxford Univ. Press
  52. Moore J. 52.  2012. A history of parasites and hosts, science and fashion. See Ref. 32 1–14
  53. Moreau SJ, Asgari S. 53.  2015. Venom proteins from parasitoid wasps and their biological functions. Toxins 7:2385–412 [Google Scholar]
  54. Mrinalini, Werren JH. 54.  2017. Parasitoid wasps and their venoms. Evolution of Venomous Animals and Their Toxins A Malhotra 187–212 Dordrecht, Neth.: Springer Sci. Bus. Media Dordrecht [Google Scholar]
  55. Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J. 55.  et al. 2002. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu. Rev. Entomol. 47:733–71 [Google Scholar]
  56. Poulin R. 56.  2011. Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior HJ Brockmann 151–86 Burlington, VT: Elsevier [Google Scholar]
  57. Romig T, Lucius R, Frank W. 57.  1980. Cerebral larvae in the second intermediate host of Dicrocoelium dendriticum (Rudolphi, 1819) and Dicrocoelium hospes looss, 1907 (Trematodes, Dicrocoeliidae).. Z. Für Parasitenkd. 63:277–86 [Google Scholar]
  58. Roseler PF, Roseler I, Strambi A, Augier R. 58.  1984. Influence of insect hormones on the establishment of dominance hierarchies among foundresses of the paper wasp, Polistes gallicus. Behav. Ecol. Sociobiol. 15:133–42 [Google Scholar]
  59. Rosenberg LA, Pflüger HJ, Wegener G, Libersat F. 59.  2006. Wasp venom injected into the prey's brain modulates thoracic identified monoaminergic neurons. J. Neurobiol. 66:155–68 [Google Scholar]
  60. Sato T, Watanabe K, Kanaiwa M, Niizuma Y, Harada Y, Lafferty KD. 60.  2011. Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92:201–7 [Google Scholar]
  61. Shi M, Dong S, Li M-t, Yang Y-y, Stanley D, Chen X-x. 61.  2015. The endoparasitoid, Cotesia vestalis, regulates host physiology by reprogramming the neuropeptide transcriptional network. Sci. Rep. 5:8173 [Google Scholar]
  62. Strambi A, Strambi C. 62.  1973. Influence du développement du paraiste Xenos vesparum Rossi (Insecte, Strepsitere) sur le systéme neuroendocrinien des femelles de Polistes (Hyménoptère, Vepside) au debut de leur vie imaginale. Arch. Anatomie Microsc. Morphol. Exp. 62:39–54 [Google Scholar]
  63. Takasuka K, Yasui T, Ishigami T, Nakata K, Matsumoto R. 63.  et al. 2015. Host manipulation by an ichneumonid spider ectoparasitoid that takes advantage of preprogrammed web-building behaviour for its cocoon protection. J. Exp. Biol. 218:2326–32 [Google Scholar]
  64. Thomas F, Schmidt-Rhaesa A, Martin G, Manu C, Durand P, Renaud F. 64.  2002. Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?. J. Evol. Biol. 15:356–61 [Google Scholar]
  65. Triltsch H. 65.  1996. On the parasitization of the ladybird Coccinella septempunctata L. (Col., Coccinellidae). J. Appl. Entomol. 120:375–78 [Google Scholar]
  66. Van Houte S, Ros VI, Oers MM. 66.  2013. Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. Mol. Ecol. 22:3458–75 [Google Scholar]
  67. Vilhelmsen L, Isidoro N, Romani R, Basibuyuk HH, Quicke DL. 67.  2001. Host location and oviposition in a basal group of parasitic wasps: the subgenual organ, ovipositor apparatus and associated structures in the Orussidae (Hymenoptera, Insecta). Zoomorphology 121:63–84 [Google Scholar]
  68. Weinersmith KL, Liu SM, Forbes AA, Egan SP. 68.  2017. Tales from the crypt: a parasitoid manipulates the behaviour of its parasite host. Proc. R. Soc. B 284:20162365 [Google Scholar]
  69. Weisel-Eichler A, Haspel G, Libersat F. 69.  1999. Venom of a parasitoid wasp induces prolonged grooming in the cockroach. J. Exp. Biol. 202:957–64 [Google Scholar]
  70. Žitňan D, Kingan TG, Kramer SJ, Beckage NE. 70.  1995. Accumulation of neuropeptides in the cerebral neurosecretory system of Manduca sexta larvae parasitized by the braconid wasp Cotesia congregata.. J. Comp. Neurol. 356:83–100 [Google Scholar]
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