Parasites: Evolution's neurobiologists

Journal of Experimental Biology

Volumn 216, Issue 1, 2013, Pages 3-10

  Adamo, Shelley Anne ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Brain; Host behaviour; Manduca; Nervous system; Parasitic manipulation; Psychoneuroimmunology; Wasp

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; BEHAVIOR; BRAIN; EVOLUTION; GENOMICS; HOST PARASITE INTERACTION; HUMAN; IMMUNE SYSTEM; IMMUNOMODULATION; NEUROSCIENCE; PARASITE; PARASITOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; BEHAVIOR; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BRAIN; GENOMICS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNE SYSTEM; NEUROIMMUNOMODULATION; NEUROSCIENCES; PARASITES;

MANDUCA;

EID: 84871180561     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.073601     Document Type: Review

References (93)

1. Abbott, A. (2011). Novartis to shut brain research facility. Nature 480, 161-162.
2. Adamantidis, A. R., Tsai, H. C., Boutrel, B., Zhang, F., Stuber, G. D., Budygin, E. A., Touriño, C., Bonci, A., Deisseroth, K. and de Lecea, L. (2011). Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J. Neurosci. 31, 10829-10835.
3. Adamo, S. A. (1997). How parasites alter the behaviour of their insect hosts. In Parasites and Pathogens. Effects on Host Hormones and Behavior (ed. N. Beckage), pp. 231-245. New York, NY: Chapman and Hall.
4. Adamo, S. A. (1998). Feeding suppression in the tobacco hornworm, Manduca sexta: costs and benefits to the parasitic wasp Cotesia congregata. Can. J. Zool. 76, 1634-1640.
5. Adamo, S. A. (2002). Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain Behav. Evol. 60, 370-377.
6. Adamo, S. A. (2005). Parasitic suppression of feeding in the tobacco hornworm, Manduca sexta: parallels with feeding depression after an immune challenge. Arch. Insect Biochem. Physiol. 60, 185-197.
7. Adamo, S. A. (2006). Comparative psychoneuroimmunology: evidence from the insects. Behav. Cogn. Neurosci. Rev. 5, 128-140.
8. Adamo, S. A. (2008a). Bidirectional connections between the immune system and the nervous system in insects. In Insect Immunology (ed. N. E. Beckage), pp. 129-149. San Diego, CA: Academic Press.
9. Adamo, S. A. (2008b). Norepinephrine and octopamine: linking stress and immune function across phyla. Invertebrate Surviv. J. 5, 12-19.
10. Adamo, S. A. (2010). Why should an immune response activate the stress response? Insights from the insects (the cricket Gryllus texensis). Brain Behav. Immun. 24, 194-200.
11. Adamo, S. A. (2012). The strings of the puppet master: how parasites change host behaviour. In Parasitic Manipulation (ed. D. Hughes and F. Thomas), pp. 36-51. Oxford: Oxford University Press.
12. Adamo, S. A. and Shoemaker, K. L. (2000). Effects of parasitism on the octopamine content of the central nervous system of Manduca sexta: A possible mechanism underlying host behavioural change. Can. J. Zool. 78, 1580-1587.
13. Adamo, S. A., Linn, C. E. and Beckage, N. E. (1997). Correlation between changes in host behaviour and octopamine levels in the tobacco hornworm Manduca sexta parasitized by the gregarious braconid parasitoid wasp Cotesia congregata. J. Exp. Biol. 200, 117-127.
14. Aubert, A. (1999). Sickness and behaviour in animals: A motivational perspective. Neurosci. Biobehav. Rev. 23, 1029-1036.
15. Beckage, N. E. (1997). New insights: how parasites and pathogens alter the endocrine physiology and development of insect hosts. In Parasites and Pathogens: Effects on Host Hormones and Behavior (ed. N. E. Beckage), pp. 3-36. New York, NY: Chapman & Hall.
16. Benito, E., Valor, L. M., Jimenez-Minchan, M., Huber, W. and Barco, A. (2011). cAMP response element-binding protein is a primary hub of activity-driven neuronal gene expression. J. Neurosci. 31, 18237-18250.
17. Bentivoglio, M., Mariotti, R. and Bertini, G. (2011). Neuroinflammation and brain infections: historical context and current perspectives. Brain Res. Rev. 66, 152-173.
18. Berenreiterová, M., Flegr, J., Kubena, A. A. and Nemec, P. (2011). The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: implications for the behavioral manipulation hypothesis. PLoS ONE 6, e28925.
19. Biron, D. G. and Loxdale, H. D. (2013). Host-parasite molecular cross-talk during the manipulative process of a host by its parasite. J. Exp. Biol. 216, 148-160.
20. Biron, D. G., Marché, L., Ponton, F., Loxdale, H. D., Galéotti, N., Renault, L., Joly, C. and Thomas, F. (2005). Behavioural manipulation in a grasshopper harbouring hairworm: A proteomics approach. Proc. Biol. Sci. 272, 2117-2126.
21. Biron, D. G., Ponton, F., Marché, L., Galeotti, N., Renault, L., Demey-Thomas, E., Poncet, J., Brown, S. P., Jouin, P. and Thomas, F. (2006). 'Suicide' of crickets harbouring hairworms: A proteomics investigation. Insect Mol. Biol. 15, 731-742.
22. Boucias, D. G. and Pendland, J. C. (1998). Principles of Insect Pathology. Boston, MA: Kluwer.
23. Bousquet, F., Nojima, T., Houot, B., Chauvel, I., Chaudy, S., Dupas, S., Yamamoto, D. and Ferveur, J. F. (2012). Expression of a desaturase gene, desat1, in neural and nonneural tissues separately affects perception and emission of sex pheromones in Drosophila. Proc. Natl. Acad. Sci. USA 109, 249-254.
24. Brembs, B., Christiansen, F., Pflüger, H. J. and Duch, C. (2007). Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J. Neurosci. 27, 11122-11131.
25. Carew, T. J. (2000). Behavioral Neurobiology. Sunderland, MA: Sinauer.
26. Cézilly, F. and Perrot-Minnot, M. J. (2005). Studying adaptive changes in the behaviour of infected hosts: A long and winding road. Behav. Processes 68, 223-228.
27. Cooper, J. R., Bloom, F. E. and Roth, R. R. (2003). The Biochemical Basis of Neuropharmacology. New York, NY: Oxford University Press.
28. Cossart, P. (2011). Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl. Acad. Sci. USA 108, 19484-19491.
29. Dantzer, R. (2004). Cytokine-induced sickness behaviour: A neuroimmune response to activation of innate immunity. Eur. J. Pharmacol. 500, 399-411.
30. Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W. and Kelley, K. W. (2008). From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9, 46-56.
31. de Jong-Brink, M. (1995). How schistosomes profit from the stress responses they elicit in their hosts. Adv. Parasitol. 35, 177-256.
32. de Jong-Brink, M., Hoek, R., Lageweg, W. and Smit, A. (1997). Schistosome parasites induce physiological changes in their snail host by interfering with two regulatory systems, the internal defense system and the neuroendocrine system. In Parasites and Pathogens. Effects on Host Hormones and Behavior (ed. N. Beckage), pp. 57-75. New York, NY: Chapman and Hall.
33. de Jong-Brink, M., Bergamin-Sassen, M. and Solis Soto, M. (2001). Multiple strategies of schistosomes to meet their requirements in the intermediate snail host. Parasitology 123, S129-S141.
34. Eberhard, W. G. (2010). Recovery of spiders from the effects of parasitic wasps: implications for fine-tuned mechanisms of manipulation. Anim. Behav. 79, 375-383.
35. Eskow Jaunarajs, K. L., Angoa-Perez, M., Kuhn, D. M. and Bishop, C. (2011). Potential mechanisms underlying anxiety and depression in Parkinson's disease: consequences of L-DOPA treatment. Neurosci. Biobehav. Rev. 35, 556-564.
36. Feener, D. H., Jr and Brown, B. V. (1997). Diptera as parasitoids. Annu. Rev. Entomol. 42, 73-97.
37. Friberg, I. M., Bradley, J. E. and Jackson, J. A. (2010). Macroparasites, innate immunity and immunoregulation: developing natural models. Trends Parasitol. 26, 540-549.
38. Gal, R. and Libersat, F. (2008). A parasitoid wasp manipulates the drive for walking of its cockroach prey. Curr. Biol. 18, 877-882.
39. Gilmore, T. D. (2006). Introduction to NF-?B: players, pathways, perspectives. Oncogene 25, 6680-6684.
40. Godfray, H. C. J. (1994). Parasitoids. Princeton, NJ: Princeton University Press.
41. Gonzalez L. E., Rojnik, B., Urrea, F., Urdaneta, H., Petrosino, P., Colasante, C., Pino, S. and Hernandez, L. (2007). Toxoplasma gondii infection lower anxiety as measured in the plus-maze and social interaction tests in rats: A behavioral analysis Behav. Brain Res. 177, 70-79.
42. Hakimi, M. A. and Cannella, D. (2011). Apicomplexan parasites and subversion of the host cell microRNA pathway. Trends Parasitol. 27, 481-486.
43. Hart, B. L. (1988). Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12, 123-137.
44. Hayakawa, Y., Ohnishi, A., Mizoguchi, A. and Yamashika, C. (2000). Distribution of growth-blocking peptide in the insect central nervous tissue. Cell Tissue Res. 300, 459-464.
45. Helluy, S. (2013). Parasite-induced alterations of sensorimotor pathways in gammarids: collateral damage of neuroinflammation? J. Exp. Biol. 216, 67-77.
46. Helluy, S. and Thomas, F. (2003). Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda). Proc. Biol. Sci. 270, 563-568.
47. Helluy, S. and Thomas, F. (2010). Parasitic manipulation and neuroinflammation: evidence from the system Microphallus papillorobustus (Trematoda) - Gammarus (Crustacea). Parasit. Vectors 3, 38-49.
48. Hoover, K., Grove, M., Gardner, M., Hughes, D. P., McNeil, J. and Slavicek, J. (2011). A gene for an extended phenotype. Science 333, 1401-1401.
49. Huber, R. (2005). Amines and motivated behaviors: A simpler systems approach to complex behavioral phenomena. J. Comp. Physiol. A 191, 231-239.
50. Hughes, D. P., Wappler, T. and Labandeira, C. C. (2011). Ancient death-grip leaf scars reveal ant-fungal parasitism. Biol. Lett. 7, 67-70.
51. Klein, S. L. (2003). Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol. Behav. 79, 441-449.
52. Laothamatas, J., Wacharapluesadee, S., Lumlertdacha, B., Ampawong, S., Tepsumethanon, V., Shuangshoti, S., Phumesin, P., Asavaphatiboon, S., Worapruekjaru, L., Avihingsanon, Y. et al. (2008). Furious and paralytic rabies of canine origin: neuroimaging with virological and cytokine studies. J. Neurovirol. 14, 119-129.
53. Lefèvre, T., Adamo, S. A., Biron, D. G., Missé, D., Hughes, D. and Thomas, F. (2009). Invasion of the body snatchers: The diversity and evolution of manipulative strategies in host-parasite interactions. Adv. Parasitol. 68, 45-83.
54. Libersat, F. and Gal, R. (2013). What can parasitoid wasps teach us about decisionmaking in insects? J. Exp. Biol. 216, 47-55.
55. Libersat, F., Delago, A. and Gal, R. (2009). Manipulation of host behavior by parasitic insects and insect parasites. Annu. Rev. Entomol. 54, 189-207.
56. Maure, F., Brodeur, J., Ponlet, N., Doyon, J., Firlej, A., Elguero, E. and Thomas, F. (2011). The cost of a bodyguard. Biol. Lett. 7, 843-846.
57. McDonough, K. A. and Rodriguez, A. (2012). The myriad roles of cyclic AMP in microbial pathogens: from signal to sword. Nat. Rev. Microbiol. 10, 27-38.
58. Meffert, M. K., Chang, J. M., Wiltgen, B. J., Fanselow, M. S. and Baltimore, D. (2003). NF-?B functions in synaptic signaling and behavior. Nat. Neurosci. 6, 1072-1078.
59. Miles, C. I. and Booker, R. (2000). Octopamine mimics the effects of parasitism on the foregut of the tobacco hornworm Manduca sexta. J. Exp. Biol. 203, 1689-1700.
60. Monastirioti, M., Linn, C. E., Jr and White, K. (1996). Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J. Neurosci. 16, 3900-3911.
61. Moore, J. (2002). Parasites and the Behavior of Animals. New York, NY: Oxford University Press.
62. Nation, J. L. (2008). Insect Physiology and Biochemistry. Boca Raton, FL: CRC Press.
63. O'Reilly, D. R. (1995). Baculovirus-encoded ecdysteroid udp-glucosyltransferases. Insect Biochem. Mol. Biol. 25, 541-550.
64. O'Reilly, D. R., Brown, M. R. and Miller, L. K. (1992). Alteration of ecdysteroid metabolism due to baculovirus infection of the fall armyworm Spodoptera frugiperda: host ecdysteroids are conjugated with galactose. Insect Biochem. Mol. Biol. 22, 313-320.
65. Ottaviani, E. and Franceschi, C. (1996). The neuroimmunology of stress from invertebrates to man. Prog. Neurobiol. 48, 421-440.
66. Perrot-Minnot, M.-J. and Cézilly, F. (2013). Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects. J. Exp. Biol. 216, 134-141.
67. Ponton, F., Lefèvre, T., Lebarbenchon, C., Thomas, F., Loxdale, H. D., Marché, L., Renault, L., Perrot-Minnot, M. J. and Biron, D. G. (2006). Do distantly related parasites rely on the same proximate factors to alter the behaviour of their hosts? Proc. Biol. Sci. 273, 2869-2877.
68. Poulin, R. (2010). Parasite manipulation of host behavior: An update and frequently asked questions. Adv. Stud. Behav. 41, 151-186.
69. Prandovszky, E., Gaskell, E., Martin, H., Dubey, J. P., Webster, J. P. and McConkey, G. A. (2011). The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE 6, e23866.
70. Pryor, S. C. and Elizee, R. (2000). Evidence of opiates and opioid neuropeptides and their immune effects in parasitic invertebrates representing three different phyla: Schistosoma mansoni, Theromyzon tessulatum, Trichinella spiralis. Acta Biol. Hung. 51, 331-341.
71. Purves, D., Augustine, G. J., Fitzpatrick, D., Hall, W. C., LaMantia, A. S. and White, L. E. (2012). Neuroscience, 5th edn. Sunderland, MA: Sinauer.
72. Rahman, M. M. and McFadden, G. (2011). Modulation of NF-?B signalling by microbial pathogens. Nat. Rev. Microbiol. 9, 291-306.
73. Roberts, L. S. and Janovy, J. (1996). Foundations of Parasitology. Boston, MA: WCB.
74. Rosenberg, L. A., Glusman, J. G. and Libersat, F. (2007). Octopamine partially restores walking in hypokinetic cockroaches stung by the parasitoid wasp Ampulex compressa. J. Exp. Biol. 210, 4411-4417.
75. Schmid-Hempel, P. (2011). Evolutionary Parasitology. New York, NY: Oxford University Press.
76. Skinner, W. S., Dennis, P. A., Li, J. P., Summerfelt, R. M., Carney, R. L. and Quistad, G. B. (1991). Isolation and identification of paralytic peptides from hemolymph of the lepidopteran insects Manduca sexta, Spodoptera exigua, and Heliothis virescens. J. Biol. Chem. 266, 12873-12877.
77. Sombati, S. and Hoyle, G. (1984). Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. J. Neurobiol. 15, 481-506.
78. Spindler, K. D., Hönl, C., Tremmel, C., Braun, S., Ruff, H. and Spindler-Barth, M. (2009). Ecdysteroid hormone action. Cell. Mol. Life Sci. 66, 3837-3850.
79. Steel, C. G. H. and Vafopoulou, X. (2006). Circadian orchestration of developmental hormones in the insect, Rhodnius prolixus. Comp. Biochem. Physiol. 144A, 351-364.
80. Thanomsridetchai, N., Singhto, N., Tepsumethanon, V., Shuangshoti, S., Wacharapluesadee, S., Sinchaikul, S., Chen, S. T., Hemachudha, T. and Thongboonkerd, V. (2011). Comprehensive proteome analysis of hippocampus, brainstem, and spinal cord from paralytic and furious dogs naturally infected with rabies. J. Proteome Res. 10, 4911-4924.
81. Thomas, F., Adamo, S. A. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behav. Processes 68, 185-199.
82. Venken, K. J. T., Simpson, J. H. and Bellen, H. J. (2011). Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72, 202-230.
83. Vyas, A. (2013). Parasite-augmented mate choice and reduction in innate fear in rats infected by Toxoplasma gondii. J. Exp. Biol. 216, 120-126.
84. Weaver, I. C. G. (2011). Toward an understanding of the dynamic interdependence of genes and environment in the regulation of phenotype. In Brain, Behavior, and Epigenetics (ed. A. Petronis and J. Mill), pp. 209-243. Berlin: Springer-Verlag.
85. Webster, J. P., Brunton, C. F. A. and MacDonald, D. W. (1994). Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology 109, 37-43.
86. Webster, J. P., Lamberton, P. H. L., Donnelly, C. A. and Torrey, E. F. (2006). Parasites as causative agents of human affective disorders? The impact of antipsychotic, mood-stabilizer and anti-parasite medication on Toxoplasma gondii's ability to alter host behaviour. Proc. Biol. Sci. 273, 1023-1030.
87. Webster, J. P., Kaushik, M., Bristow, G. C. and McConkey, G. A. (2013). Toxoplasma gondii infection, from predation to schizophrenia: can animal behaviour help us understand human behaviour? J. Exp. Biol. 216, 99-112.
88. Weiger, W. A. (1997). Serotonergic modulation of behaviour: A phylogenetic overview. Biol. Rev. Camb. Philos. Soc. 72, 61-95.
89. Weinberger, D. R., Harrison, P. J., Haddad, P. M. and Mattay, V. S. (2011). Neurological complications of antipsychotic drugs. In Schizophrenia (ed. D. R. Weinberger and P. J. Harrison), pp. 561-576. Chichester, UK: Wiley-Blackwell.
90. Weisel-Eichler, A. and Libersat, F. (2004). Venom effects on monoaminergic systems. J. Comp. Physiol. A 190, 683-690.
91. Yu, X. Q., Prakash, O. and Kanost, M. R. (1999). Structure of a paralytic peptide from an insect, Manduca sexta. J. Pept. Res. 54, 256-261.
92. Zalcman, S. S. and Siegel, A. (2006). The neurobiology of aggression and rage: role of cytokines. Brain Behav. Immun. 20, 507-514.
93. Zitnan, D., Kingan, T. G., Kramer, S. J. and Beckage, N. E. (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.