1932

Abstract

Humans, wildlife, and domestic animals are intimately linked through shared infections. Many parasites and pathogens use multiple host species, either opportunistically or sequentially, such that managing disease risk frequently requires a broader understanding of the ecological community. The coccidian protozoan infects more than one hundred species of vertebrates, ranging from bats to beluga whales. In humans, acute toxoplasmosis can have serious health consequences for immunocompromised individuals. Even amongst asymptomatic patients, however, toxoplasmosis has been linked to a range of behavioral alterations and conditions, such as changes in risk tolerance, neuroticism, mental illness, suicide, and accident proneness. Whether such links are causal or simply correlational has been the subject of intense study and debate; from an evolutionary standpoint, selection may favor parasite-induced alterations in host behavior that increase the likelihood a host is consumed by the definitive host—in this case a domestic or wild felid. Here, we examine current evidence for parasite-induced manipulations of host behavior, in both humans and other animals. We critically evaluate proposed mechanisms through which infection might influence host behavior, which range from inflammation in the brain to changes in hormones or neurotransmitters. Considering estimates that may infect up to one-third of the global human population, we conclude by examining the implications of these changes for human behavior, individual fitness, and emergent cultural properties.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-081720-111125
2021-02-15
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/animal/9/1/annurev-animal-081720-111125.html?itemId=/content/journals/10.1146/annurev-animal-081720-111125&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Woolhouse ME, Webster JP, Domingo E, Charlesworth B, Levin BR 2002. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32:4569–77
    [Google Scholar]
  2. 2. 
    Jones KE, Patel NG, Levy MA, Storeygard A, Balk D et al. 2008. Global trends in emerging infectious diseases. Nature 451:7181990–93
    [Google Scholar]
  3. 3. 
    Messenger AM, Barnes AN, Gray GC 2014. Reverse zoonotic disease transmission (zooanthroponosis): a systematic review of seldom-documented human biological threats to animals. PLOS ONE 9:e89055
    [Google Scholar]
  4. 4. 
    Daszak P, Cunningham AA, Hyatt AD 2000. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–49
    [Google Scholar]
  5. 5. 
    Gebreyes WA, Dupouy-Camet J, Newport MJ, Oliveira CJ, Schlesinger LS et al. 2014. The Global One Health paradigm: challenges and opportunities for tackling infectious diseases at the human, animal, and environment interface in low-resource settings. PLOS Negl. Trop. Dis. 8:e3257
    [Google Scholar]
  6. 6. 
    Porter SB, Sande MA. 1992. Toxoplasmosis of the central nervous system in the acquired immunodeficiency syndrome. N. Engl. J. Med. 327:1643–48
    [Google Scholar]
  7. 7. 
    Kravetz JD, Federman DG. 2005. Toxoplasmosis in pregnancy. Am. J. Med. 118:212–16
    [Google Scholar]
  8. 8. 
    Mikaelian I, Boisclair J, Dubey JP, Kennedy S, Martineau D 2000. Toxoplasmosis in beluga whales (Delphinapterusleucas) from the St. Lawrence Estuary: two case reports and a serological survey. J. Comp. Pathol. 122:73–76
    [Google Scholar]
  9. 9. 
    Dubey JP. 2010. Toxoplasmosis of Animals and Humans Boca Raton, FL: CRC Press 2nd ed.
  10. 10. 
    Lindsay DS, Dubey JP. 2020. Toxoplasmosis in wild and domestic animals. Toxoplasma gondii, ed. LM Weiss, K Kim 293–320 Cambridge, MA: Academic
  11. 11. 
    Houdek P. 2017. Puppet master: possible influence of the parasite Toxoplasmagondii on managers and employees. Acad. Manag. Perspect. 31:163–81
    [Google Scholar]
  12. 12. 
    House PK, Vyas A, Sapolsky R 2011. Predator cat odors activate sexual arousal pathways in brains of Toxoplasmagondii infected rats. PLOS ONE 6:e23277
    [Google Scholar]
  13. 13. 
    Flegr J. 2013. How and why Toxoplasma makes us crazy. Trends Parasitol 29:4156–63
    [Google Scholar]
  14. 14. 
    Conrad PA, Miller MA, Kreuder C, James ER, Mazet J et al. 2005. Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasmagondii flow into the marine environment. Int. J. Parasitol. 35:1155–68
    [Google Scholar]
  15. 15. 
    Hollings T, Jones M, Mooney N, McCallum H 2013. Wildlife disease ecology in changing landscapes: mesopredator release and toxoplasmosis. Int. J. Parasitol. 2:110–18
    [Google Scholar]
  16. 16. 
    Dubey JP. 2020. The history and life cycle of Toxoplasmagondii. Toxoplasma gondii, ed. LM Weiss, K Kim 1–19 Cambridge, MA: Academic
  17. 17. 
    Martorelli Di Genova B, Wilson SK, Dubey JP, Knoll LJ 2019. Intestinal delta-6-desaturase activity determines host range for Toxoplasma sexual reproduction. PLOS Biol 17:8e3000364
    [Google Scholar]
  18. 18. 
    Dubey JP. 1996. Infectivity and pathogenicity of Toxoplasmagondii oocysts for cats. J. Parasitol. 82:957–60
    [Google Scholar]
  19. 19. 
    Dubey JP, Frenkel JK. 1976. Feline toxoplasmosis from acutely infected mice and the development of Toxoplasma cysts. J. Protozool. 23:537–46
    [Google Scholar]
  20. 20. 
    Levaditi C, Schoen R, Sanchis Bayarri V 1928. L'encéphalomyélite toxoplasmique chronique du lapin et de la souris. C. R. Soc. Biol. 99:37–40
    [Google Scholar]
  21. 21. 
    Dubey JP. 1998. Reexamination of resistance of Toxoplasmagondii tachyzoites to pepsin digestion. Parasitology 116:43–50
    [Google Scholar]
  22. 22. 
    Dubey JP. 1997. Bradyzoites-induced murine toxoplasmosis: stage conversion, pathogenesis, and tissue cyst formation in mice fed bradyzoites of different strains of Toxoplasmagondii. J. Eukaryot. Microbiol 44:592–602
    [Google Scholar]
  23. 23. 
    Ferguson DJP, Huskinson-Mark J, Araujo FG, Remington JS 1994. A morphological study of chronic cerebral toxoplasmosis in mice: comparison of four different strains of Toxoplasmagondii. Parasitol. Res 80:493–501
    [Google Scholar]
  24. 24. 
    Dass SAH, Vasudevan A, Dutta D, Soh LJT, Sapolsky RM, Vyas A 2011. Protozoan parasite Toxoplasmagondii manipulates mate choice in rats by enhancing attractiveness of males. PLOS ONE 6:11e27229
    [Google Scholar]
  25. 25. 
    Arantes TP, Lopes WDZ, Ferreira RM, Pieroni JSP, Pinto VM et al. 2009. Toxoplasmagondii: evidence for the transmission by semen in dogs. Exp. Parasitol. 123:2190–94
    [Google Scholar]
  26. 26. 
    Gutierrez J, O'Donovan J, Williams E, Proctor A, Brady C et al. 2010. Detection and quantification of Toxoplasmagondii in ovine maternal and foetal tissues from experimentally infected pregnant ewes using real-time PCR. Vet. Parasitol. 172:1–28–15
    [Google Scholar]
  27. 27. 
    Flegr J, Klapilová K, Kaňková Š 2014. Toxoplasmosis can be a sexually transmitted infection with serious clinical consequences. Not all routes of infection are created equal. Med. Hypotheses 83:3286–89
    [Google Scholar]
  28. 28. 
    Beverley JKA. 1959. Congenital transmission of toxoplasmosis through successive generations of mice. Nature 183:46711348–49
    [Google Scholar]
  29. 29. 
    Moore J. 2002. Parasites and the Behavior of Animals Oxford, UK: Oxford Univ. Press
  30. 30. 
    Poulin R. 2010. Parasite manipulation of host behavior: an update and frequently asked questions. Adv. Study Behav. 41:151–86
    [Google Scholar]
  31. 31. 
    Lafferty KD, Morris KA. 1996. Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390–97
    [Google Scholar]
  32. 32. 
    Gatkowska J, Wieczorek M, Dziadek B, Dzitko K, Dlugonska H 2012. Behavioral changes in mice caused by Toxoplasmagondii invasion of brain. Parasitol. Res. 111:153–58
    [Google Scholar]
  33. 33. 
    Berdoy M, Webster JP, Macdonald DW 2000. Fatal attraction in rats infected with Toxoplasmagondii. Proc. R. Soc. B 267:14521591–94
    [Google Scholar]
  34. 34. 
    Vyas A, Kim S-K, Giacomini N, Boothroyd JC, Sapolsky RM 2007. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. PNAS 104:156442–47
    [Google Scholar]
  35. 35. 
    Kaushik M, Knowles SCL, Webster JP 2014. What makes a feline fatal in Toxoplasmagondii’s fatal feline attraction? Infected rats choose wild cats. Am. Zool 542118–28
  36. 36. 
    Boillat M, Hammoudi PM, Dogga SK, Pagès S, Goubran M et al. 2020. Neuroinflammation-associated aspecific manipulation of mouse predator fear by Toxoplasmagondii. Cell Rep 30:2320–34
    [Google Scholar]
  37. 37. 
    Bezerra ECM, dos Santos SV, Coelho dos Santos TC, de Andrade HF Jr., Meireles LR 2019. Behavioral evaluation of BALB/c (Musmusculus) mice infected with genetically distinct strains of Toxoplasmagondii. Microb. Pathog 126:279–86
    [Google Scholar]
  38. 38. 
    Poirotte C, Kappeler PM, Ngoubangoye B, Bourgeois S, Moussodji M, Charpentier MJ 2016. Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees. Curr. Biol. 26:3R98–R99
    [Google Scholar]
  39. 39. 
    Flegr J, Lenochová P, Hodný Z, Vondrová M 2011. Fatal attraction phenomenon in humans—cat odour attractiveness increased for Toxoplasma-infected men while decreased for infected women. PLOS Negl. Trop. Dis. 5:11e1389
    [Google Scholar]
  40. 40. 
    Gajewski PD, Falkenstein M, Hengstler JG, Golka K 2014. Toxoplasmagondii impairs memory in infected seniors. Brain Behav. Immun. 36:193–99
    [Google Scholar]
  41. 41. 
    Stock A-K, Dajkic D, Köhling HL, von Heinegg EH, Fiedler M, Beste C 2017. Humans with latent toxoplasmosis display altered reward modulation of cognitive control. Sci. Rep. 7:10170
    [Google Scholar]
  42. 42. 
    Flegr J, Havlícek J, Kodym P, Malý M, Smahel Z 2002. Increased risk of traffic accidents in subjects with latent toxoplasmosis: a retrospective case-control study. BMC Infect. Dis. 2:11
    [Google Scholar]
  43. 43. 
    Yagmur F, Yazar S, Temel HO, Cavusoglu M 2010. May Toxoplasmagondii increase suicide attempt—preliminary results in Turkish subjects?. Forensic Sci. Int. 199:15–17
    [Google Scholar]
  44. 44. 
    Gohardehi S, Sharif M, Sarvi S, Moosazadeh M, Alizadeh-Navaei R et al. 2018. The potential risk of toxoplasmosis for traffic accidents: a systematic review and meta-analysis. Exp. Parasitol. 191:19–24
    [Google Scholar]
  45. 45. 
    Samojłowicz D, Twarowska-Małczyńska J, Borowska-Solonynko A, Poniatowski ŁA, Sharma N, Olczak M 2019. Presence of Toxoplasmagondii infection in brain as a potential cause of risky behavior: a report of 102 autopsy cases. Eur. J. Clin. Microbiol. Infect. Dis. 38:2305–17
    [Google Scholar]
  46. 46. 
    Ling VJ, Lester D, Mortensen PB, Langenberg PW, Postolache TT 2011. Toxoplasmagondii seropositivity and suicide rates in women. J. Nerv. Ment. Dis. 199:7440–44
    [Google Scholar]
  47. 47. 
    Soleymani E, Faizi F, Heidarimoghadam R, Davoodi L, Mohammadi Y 2020. Association of T.gondii infection with suicide: a systematic review and meta-analysis. BMC Public Health 20:766
    [Google Scholar]
  48. 48. 
    Sugden K, Moffitt TE, Pinto L, Poulton R, Williams BS, Caspi A 2016. Is Toxoplasmagondii infection related to brain and behavior impairments in humans? Evidence from a population-representative birth cohort. PLOS ONE 11:2e0148435
    [Google Scholar]
  49. 49. 
    Sutterland AL, Fond G, Kuin A, Koeter MWJ, Lutter R et al. 2015. Beyond the association. Toxoplasmagondii in schizophrenia, bipolar disorder, and addiction: systematic review and meta‐analysis. Acta Psychiatr. Scand. 132:3161–79
    [Google Scholar]
  50. 50. 
    Arias I, Sorlozano A, Villegas E, de Dios Luna J, McKenney K et al. 2012. Infectious agents associated with schizophrenia: a meta-analysis. Schizophr. Res. 136:1–3128–36
    [Google Scholar]
  51. 51. 
    Alvarado-Esquivel C, Sánchez-Anguiano LF, Hernández-Tinoco J, Berumen-Segovia LO, Torres-Prieto YE et al. 2016. Toxoplasmagondii infection and depression: a case-control seroprevalence study. Eur. J. Microbiol. Immunol. 6:285–89
    [Google Scholar]
  52. 52. 
    Wadhawan A, Daue ML, Brenner LA, Lowry CA, Dagdag A et al. 2018. ToxoplasmaGondii-oocyst seropositivity and depression in the Old Order Amish. Biol. Psychiatry 83:9S299–S300
    [Google Scholar]
  53. 53. 
    Hamdani N, Daban-Huard C, Lajnef M, Richard JR, Delavest M et al. 2013. Relationship between Toxoplasmagondii infection and bipolar disorder in a French sample. J. Affect. Dis. 148:2–3444–48
    [Google Scholar]
  54. 54. 
    Miman O, Mutlu EA, Ozcan O, Atambay M, Karlidag R, Unal S 2010. Is there any role of Toxoplasmagondii in the etiology of obsessive–compulsive disorder?. Psychiatry Res 177:1–2263–65
    [Google Scholar]
  55. 55. 
    Lafferty KD. 2006. Can the common brain parasite, Toxoplasmagondii, influence human culture?. Proc. R. Soc. B 273:16022749–55
    [Google Scholar]
  56. 56. 
    Maseland R. 2013. Parasitical cultures? The cultural origins of institutions and development. J. Econ. Growth 18:2109–36
    [Google Scholar]
  57. 57. 
    Johnson SK, Fitza MA, Lerner DA, Calhoun DM, Beldon MA et al. 2018. Risky business: linking Toxoplasmagondii infection and entrepreneurship behaviours across individuals and countries. Proc. R. Soc. B 285:188320180822
    [Google Scholar]
  58. 58. 
    Lerner DA, Alkærsig L, Fitza MA, Lomberg C, Johnson SK 2020. Nothing ventured, nothing gained: Parasite infection is associated with entrepreneurial initiation, engagement, and performance. Entrepreneurship 45:118–44
    [Google Scholar]
  59. 59. 
    Stibbs HH. 1985. Changes in brain concentrations of catecholamines and indoleamines in Toxoplasmagondii infected mice. Ann. Trop. Med. Parasitol. 79:2153–57
    [Google Scholar]
  60. 60. 
    Prandovszky E, Gaskell E, Martin H, Dubey JP, Webster JP, McConkey GA 2011. The neurotropic parasite Toxoplasmagondii increases dopamine metabolism. PLOS ONE6e23866
    [Google Scholar]
  61. 61. 
    Gaskell EA, Smith JE, Pinney JW, Westhead DR, McConkey GA 2009. A unique dual activity amino acid hydroxylase in Toxoplasmagondii. PLOS ONE 4:e4801
    [Google Scholar]
  62. 62. 
    Sawa A, Snyder SH. 2002. Schizophrenia: diverse approaches to a complex disease. Science 296:5568692–95
    [Google Scholar]
  63. 63. 
    Wang T, Tang ZH, Li JF, Li XN, Wang X, Zhao ZJ 2013. A potential association between Toxoplasmagondii infection and schizophrenia in mouse models. Exp. Parasitol. 135:3497–502
    [Google Scholar]
  64. 64. 
    Webster JP, McConkey GA. 2010. Toxoplasmagondii-altered host behaviour: clues as to mechanism of action. Folia Parasitol 57:295–104
    [Google Scholar]
  65. 65. 
    Ma J, He J-J, Hou J-L, Zhou C-X, Zhang F-K et al. 2019. Metabolomic signature of mouse cerebral cortex following Toxoplasmagondii infection. Parasites Vectors 12:373
    [Google Scholar]
  66. 66. 
    Notarangelo FM, Wilson EH, Horning KJ, Thomas MA, Harris TH et al. 2014. Evaluation of kyn-urenine pathway metabolism in Toxoplasmagondii-infected mice: implications for schizophrenia. Schizophr. Res. 152:261–67
    [Google Scholar]
  67. 67. 
    Okusaga O, Duncan E, Langenberg P, Brundin L, Fuchs D et al. 2016. Combined Toxoplasmagondii seropositivity and high blood kynurenine—linked with nonfatal suicidal self-directed violence in patients with schizophrenia. J. Psychiatr. Res. 72:74–81
    [Google Scholar]
  68. 68. 
    Zouei N, Shojaee S, Mohebali M, Keshavarz H 2018. The association of latent toxoplasmosis and level of serum testosterone in humans. BMC Res. Notes 11:365
    [Google Scholar]
  69. 69. 
    Flegr J, Lindová J, Kodym P 2008. Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology 135:427–31
    [Google Scholar]
  70. 70. 
    Lim A, Kumar V, Dass SAH, Vyas A 2013. Toxoplasmagondii infection enhances testicular steroidogenesis in rats. Mol. Ecol. 22:102–10
    [Google Scholar]
  71. 71. 
    Estato V, Stipursky J, Gomes F, Mergener TC, Frazão-Teixeira E et al. 2018. The neurotropic parasite Toxoplasmagondii induces sustained neuroinflammation with microvascular dysfunction in infected mice. Am. J. Pathol. 188:112674–87
    [Google Scholar]
  72. 72. 
    Novotná M, Hanusova J, Klose J, Preiss M, Havlicek J, Roubalová K et al. 2005. Probable neuroimmunological link between Toxoplasma and cytomegalovirus infections and personality changes. BMC Infect. Dis. 5:54
    [Google Scholar]
  73. 73. 
    Bay-Richter C, Petersen E, Liebenberg N, Elfving B, Wegener G 2019. Latent toxoplasmosis aggravates anxiety- and depressive-like behaviour and suggest a role of gene-environment interactions in the behavioural response to the parasite. Behav. Brain Res. 364:133–39
    [Google Scholar]
/content/journals/10.1146/annurev-animal-081720-111125
Loading
/content/journals/10.1146/annurev-animal-081720-111125
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error