When should a trophically and vertically transmitted parasite manipulate its intermediate host? The case of Toxoplasma gondii

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1765, 2013, Pages

  Lélu, Maud ^a   Langlais, Michel ^b   Poulle, Marie Lazarine ^c   Gilot Fromont, Emmanuelle ^d,e   Gandon, Sylvain ^f  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UNIVERSITÉ DE REIMS CHAMPAGNE ARDENNE   (France)

^d UNIVERSITÉ DE LYON   (France)

^e UNIVERSITÉ LYON 1   (France)

^f CNRS   (France)

Author keywords

Adaptive dynamics; Behavioural manipulation; Population genetics approach; Trophic transmission; Vertical transmission; Virulence

Indexed keywords

DISEASE TRANSMISSION; EPIDEMIC; EPIDEMIOLOGY; EVOLUTIONARY BIOLOGY; HOST-PARASITE INTERACTION; INTERMEDIATE HOST; PARASITE; POPULATION GENETICS; PREDATION; PROTOZOAN;

PROTOZOA; TOXOPLASMA GONDII;

ANIMAL; BIOLOGICAL MODEL; CAT; FEMALE; GENETICS; HOST PARASITE INTERACTION; LIFE CYCLE STAGE; MALE; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; POPULATION DYNAMICS; RAT; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; TRANSMISSION; VERTICAL TRANSMISSION; VIRULENCE;

ANIMALS; CATS; FEMALE; HOST-PARASITE INTERACTIONS; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; LIFE CYCLE STAGES; MALE; MODELS, BIOLOGICAL; POPULATION DYNAMICS; RATS; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; VIRULENCE;

EID: 84894875113     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.1143     Document Type: Article

References (53)

1. Barnard CJ, Behnke JM. 1990 Parasitism and host behaviour. London, UK: Taylor and Francis.
2. Combes C. 2001 Parasitism: the ecology and evolution of intimate interactions. Chicago, IL: University of Chicago Press.
3. Moore J. 2002 Parasites and the behaviour of animals. Oxford, UK: Oxford University Press.
4. Choisy M, Brown SP, Lafferty KD, Thomas F. 2003 Evolution of trophic transmission in parasites: why add intermediate hosts? Am. Nat. 162, 172-181. (doi:10.1086/375681)
5. Gandon S. 2004 Evolution of multihost parasites. Evolution 58, 455-469. (doi:10.1111/j.0014-3820. 2004. tb01669. x)
6. Parker GA, Ball MA, Chubb JC, Hammerschmidt K, Milinski M. 2009 When should a trophically transmitted parasite manipulate its host? Evolution 63, 448-458. (doi:10.1111/j.1558-5646.2008. 00565. x)
7. Seppälä O, Jokela J. 2008 Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biol. Lett. 4, 663-666. (doi:10.1098/rsbl.2008.0335)
8. Vervaeke M, Davis S, Leirs H, Verhagen R. 2006 Implications of increased susceptibility to predation for managing the sylvatic cycle of Echinococcus multilocularis. Parasitology 132, 893-901. (doi:10. 1017/S0031182006009838)
9. Cézilly F, Thomas F, Médoc V, Perrot-Minnot MJ. 2010 Host-manipulation by parasites with complex life cycles: adaptive or not? Trends Parasitol. 26, 311-317. (doi:10.1016/j. pt.2010.03.009)
10. Poulin R. 2010 Parasite manipulation of host behavior: an update and frequently asked questions. Adv. Stud. Behav. 41, 151-186. (doi:10.1016/ s0065-3454(10).41005-0)
11. Thomas F, Adamo S, Moore J. 2005 Parasitic manipulation: where are we and where should we go? Behav. Process. 68, 185-199. (doi:10.1016/j. beproc.2004.06.010)
12. Franceschi N, Bollache L, Cornet S, Bauer A, Motreuil S, Rigaud T. 2010 Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan-amphipod system. J. Evol. Biol. 23, 2143-2150. (doi:10.1111/j.1420-9101.2010.02076. x)
13. Thompson SN, Kavaliers M. 1994 Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109, S119-S138. (doi:10.1017/ S0031182000085139)
14. Mouritsen KN, Poulin R. 2003 Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. Int. J. Parasitol. 33, 1043-1050. (doi:10.1016/S0020-7519(03)00178-4)
15. Seppälä O, Valtonen ET, Benesh DP. 2008 Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proc. R. Soc. B 275, 1611-1615. (doi:10.1098/rspb. 2008.0152)
16. Haine ER, Boucansaud K, Rigaud T. 2005 Conflict between parasites with different transmission strategies infecting an amphipod host. Proc. R. Soc. B 272, 2505-2510. (doi:10.1098/rspb.2005.3244)
17. Jones EO, White A, Boots M. 2011 The evolution of host protection by vertically transmitted parasites. Proc. R. Soc. B 278, 863-870. (doi:10.1098/rspb.2010.1397)
18. Shoop WL. 1991 Vertical transmission of helminths: hypobiosis and amphiparatenesis. Parasitol. Today 7, 51-54. (doi:10.1016/0169-4758(91)90189-U)
19. Dubey JP. 1999 Recent advances in Neospora and neosporosis. Vet. Parasitol. 84, 349-367. (doi:10. 1016/S0304-4017(99)00044-8)
20. Tenter AM, Heckeroth AR, Weiss LM. 2000 Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30, 1217-1258. (doi:10.1016/ S0020-7519(00)00124-7)
21. Cook AJC, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, Foulon W, Semprini AE, Dunn DT, on behalf of the European Research Network on Congenital Toxoplasmosis. 2000 Sources of toxoplasma infection in pregnant women: European multicentre case-control study. BMJ 321, 142-147. (doi:10.1136/bmj.321.7254.142)
22. Gonzalez LE, Rojnik B, Urrea F, Urdaneta H, Petrosino P, Colasante C, Pino S, Hernandez L. 2007 Toxoplasma gondii infection lower anxiety as measured in the plus-maze and social interaction tests in rats: a behavioural analysis. Behav. Brain Res. 177, 70-79. (doi:10.1016/j. bbr. 2006.11.012)
23. Webster JP, Brunton CFA, MacDonald DW. 1994 Effect of Toxoplasma gondii upon neophobic behaviour in wild brown-rats, Rattus norvegicus. Parasitology 109, 37-43. (doi:10.1017/ S003118200007774X)
24. Berdoy M, Webster JP, Macdonald DW. 2000 Fatal attraction in rats infected with Toxoplasma gondii. Proc. R. Soc. Lond. B 267, 1591-1594. (doi:10. 1098/rspb.2000.1182)
25. Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM. 2007 Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odours. Proc. Natl Acad. Sci. USA 104, 6442-6447. (doi:10.1073/pnas.0608310104)
26. Lamberton PHL, Donnelly CA, Webster JP. 2008 Specificity of the Toxoplasma gondii-altered behaviour to definitive versus non-definitive host predation risk. Parasitology 135, 1143-1150. (doi:10.1017/S0031182008004666)
27. Worth AR, Lymbery AJ, Thompson RCA. 2013 Adaptive host manipulation by Toxoplasma gondii: fact or fiction? Trends Parasitol. 29, 150-155. (doi:10.1016/j. pt.2013.01.004)
28. Kannan G, Moldovan K, Xiao JC, Yolken RH, Jones-Brando L, Pletnikov MV. 2010 Toxoplasma gondii strain-dependent effects on mouse behaviour. Folia Parasitol. 57, 151-155.
29. Owen MR, Trees AJ. 1998 Vertical transmission of Toxoplasma gondii from chronically infected house (Mus musculus) and field (Apodemus sylvaticus) mice determined by polymerase chain reaction. Parasitology 116, 299-304. (doi:10.1017/ S003118209700231X)
30. Marshall PA, Hughes JM, Williams RH, Smith JE, Murphy RG, Hide G. 2004 Detection of high levels of congenital transmission of Toxoplasma gondii in natural urban populations of Mus domesticus. Parasitology 128, 39-42. (doi:10.1017/ S0031182003004189)
31. Dubey JP, Frenkel JK. 1998 Toxoplasmosis of rats: a review, with considerations of their value as an animal model and their possible role in epidemiology. Vet. Parasitol. 77, 1-32. (doi:10. 1016/S0304-4017(97)00227-6)
32. Freyre A, Falcon J, Mendez J, Rodriguez A, Correa L, Gonzalez M. 2006 Refinement of the mouse model of congenital toxoplasmosis. Exp. Parasitol. 113, 154-160. (doi:10.1016/j. exppara. 2005.12.019)
33. Freyre A, Fialho CG, Bigatti LE, Araujo FAP, Falcon JD, Mendez J, Gonzalez M. 2009 Toxoplasma gondii: congenital transmission in a hamster model. Exp. Parasitol. 122, 140-144. (doi:10.1016/j. exppara. 2009.02.004)
34. Dass SAH, Vasudevan A, Dutta D, Soh LJT, Sapolsky RM, Vyas A. 2011 Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males. PLoS ONE 6, e27229. (doi:10.1371/journal. pone.0027229)
35. Saeij JPJ, Boyle JP, Boothroyd JC. 2005 Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends Parasitol. 21, 476-481. (doi:10.1016/j. pt.2005.08.001)
36. Dardé ML. 2008 Toxoplasma gondii, 'new' genotypes and virulence. Parasite 15, 366-371. (doi:10.1051/parasite/2008153366)
37. Lélu M, Langlais M, Poulle ML, Gilot-Fromont E. 2010 Transmission dynamics of Toxoplasma gondii along an urban rural gradient. Theor. Popul. Biol. 78, 139-147. (doi:10.1016/j. tpb.2010.05.005)
38. Turner M, Lenhart S, Rosenthal B, Sullivan A, Zhao X. 2013 Modeling effective transmission pathways and control of the world's most successful parasite. Theor. Popul. Biol. 86, 50-61. (doi:10.1016/j. tpb. 2013.04)
39. Lotka AJ. 1925 Elements of physical biology. London, UK: Williams and Wilkins.
40. Volterra V. 1931 Lecons sur la théorie mathématique de la lutte pour la vie. Paris, France: Gauthier-Villars.
41. Diekmann O, Heesterbeek JAP, Metz JAJ. 1990 On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. J. Math. Biol. 28, 365-382. (doi:10.1007/BF00178324)
42. Frank SA. 1996 Models of parasite virulence. Q. Rev. Biol. 71, 37-78. (doi:10.1086/419267)
43. Day T, Gandon S. 2006 Insights from Price's equation into evolutionary epidemiology. In Disease evolution: models, concepts, and data analysis (eds Z Feng, U Dieckmann, SA Levin), pp. 23-44. Providence, RI: American Mathematical Society.
44. Day T, Gandon S. 2007 Applying population-genetic models in theoretical evolutionary epidemiology. Ecol. Lett. 10, 876-888. (doi:10.1111/j.1461-0248. 2007.01091. x)
45. Duneau D, Ebert D. 2012 Host sexual dimorphism and parasite adaptation. PLoS Biol. 10, e1001271. (doi:10.1371/journal. pbio.1001271)
46. Barragan A, Sibley LD. 2002 Transepithelial migration of Toxoplasma gondii is linked to parasite motility and virulence. J. Exp. Med. 95, 1625-1633. (doi:10.1084/jem.20020258)
47. Barragan A, Sibley LD. 2003 Migration of Toxoplasma gondii across biological barriers. Trends Microbiol. 11, 426-430. (doi:10.1016/S0966-842X(03)00205-1)
48. Freyre A, Falcon J, Mendez J, Gonzalez M, Venzal JM, Morgades D. 2003 Fetal Toxoplasma infection after oocyst inoculation of pregnant rats. Parasitol. Res. 89, 352-353. (doi:10.1007/s00436-002-0759-4)
49. Aubert D et al. 2010 Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France. Vet. Parasitol. 171, 346-349. (doi:10.1016/j. vetpar.2010.03.033)
50. Dubey JP et al. 2008 Endemic toxoplasmosis in pigs on a farm in Maryland: isolation and genetic characterization of Toxoplasma gondii. J. Parasitol. 94, 36-41. (doi:10.1645/GE-1312.1)
51. Sibley LD, Khan A, Ajioka JW, Rosenthal BM. 2009 Genetic diversity of Toxoplasma gondii in animals and humans. Phil. Trans. R. Soc. B 364, 2749-2761. (doi:10.1098/rstb.2009.0087)
52. Carme B, Demar M, Ajzenberg D, Dardé ML. 2009 Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerg. Infect. Dis. 15, 656-658. (doi:10.3201/ eid1504.081306)
53. Xiao J, Kannan G, Jones-Brando L, Brannock C, Krasnova IN, Cadet JL, Pletnikov M, Yolken RH. 2012 Sex-specific changes in gene expression and behavior induced by chronic Toxoplasma infection in mice. Neuroscience 206, 39-48. (doi:10.1016/j. neuroscience.2011.12.051)