Parasitism and the evolutionary ecology of animal personality

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1560, 2010, Pages 4077-4088

  Barber, Iain ^a   Dingemanse, Niels J ^b  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

Behavioural syndrome; Correlational selection; Parasitism; Personality; Phenotypic plasticity; Population differentiation

Indexed keywords

EVOLUTIONARY BIOLOGY; HOST-PARASITE INTERACTION; INDIVIDUAL VARIATION; LIFE HISTORY TRAIT; NATURAL SELECTION; PARASITE INFESTATION; PARASITISM; PHENOTYPIC PLASTICITY; PREDATION;

ANIMALIA;

EID: 78650591939     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0182     Document Type: Review

References (118)

1. Abbot, P. & Dill, L. M. 2001 Sexually transmitted parasites and sexual selection in the milkweed leaf beetle, Labidomera clivicollis. Oikos 92, 91-100. (doi:10.1034/j. 1600-0706.2001.920111.x)
2. Adamo, S. A. 2002 Modulating the modulators: parasites, neuromodulators and host behavioural change. Brain Behav. Evol. 60, 370-377. (doi:10.1159/000067790)
3. Anderson, R. M. & May, R. M. 1982 Coevolution of hosts and parasites. Parasitology 85, 411-426. (doi:10.1017/S0031182000055360)
4. Barber, I. 2005 Parasites grow larger in faster growing fish hosts. Int. J. Parasitol. 35, 137-143. (doi:10.1016/j. ijpara.2004.11.010)
5. Barber, I., Huntingford, F. A. & Crompton, D. W. T. 1995 The effect of hunger and cestode parasitism on the shoaling decisions of small fresh-water fish. J. Fish Biol. 47, 524-536. (doi:10.1111/j.1095-8649.1995.tb01919.x)
6. Barber, I., Walker, P. & Svensson, P. A. 2004 Behavioural responses to simulated avian predation in female three spined sticklebacks: the effect of experimental Schistocephalus solidus infections. Behaviour 141, 1425-1440. (doi:10.1163/1568539042948231)
7. Bell, A. M. 2005 Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J. Evol. Biol. 18, 464-473. (doi:10.1111/j. 1420-9101.2004.00817.x)
8. Bell, A. M. 2007 Future directions in behavioural syndromes research. Proc. R. Soc. B 274, 755-761. (doi:10.1098/rspb.2006.0199)
9. Bell, A. M. & Sih, A. 2007 Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol. Lett. 10, 828-834. (doi:10.1111/j.1461-0248.2007.01081.x)
10. Bell, A. M., Hankison, S. J. & Laskowski, K. L. 2009 The repeatability of behaviour: a meta-analysis. Anim. Behav. 77, 771-783. (doi:10.1016/j.anbehav. 2008.12.022)
11. Berdoy, M., Webster, J. P. & MacDonald, D. W. 1995 The manipulation of rat behaviour by Toxoplasma gondii. Mammalia 59, 605-613. (doi:10.1515/mamm. 1995.59.4.605)
12. Berdoy, M., Webster, J. P. & Macdonald, D. W. 2000 Fatal attraction in rats infected with Toxoplasma gondii. Proc. R. Soc. Lond. B. 267, 1591-1594. (doi:10.1098/rspb.2000.1182)
13. Biro, P. A. & Stamps, J. A. 2008 Are animal personality traits linked to life-history productivity? Trends Ecol. Evol. 23, 361-368. (doi:10.1016/j.tree.2008.04.003)
14. Blanchet, S., Mejean, L., Bourque, J. F., Lek, S., Thomas, F., Marcogliese, D. J., Dodson, J. J. & Loot, G. 2009a Why do parasitized hosts look different? Resolving the 'chicken-egg' dilemma. Oecologia 160, 37-47. (doi:10. 1007/s00442-008-1272-y)
15. Blanchet, S., Thomas, F. & Loot, G. 2009b Reciprocal effects between host phenotype and pathogens: new insights from an old problem. Trends Parasitol. 25, 364-369. (doi:10.1016/j.pt.2009.05.005)
16. Boon, A. K., Réale, D. & Boutin, S. 2007 The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecol. Lett. 10, 1094-1104. (doi:10.1111/j.1461-0248.2007.01106.x)
17. Boon, A. K., Réale, D. & Boutin, S. 2008 Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117, 1321-1328. (doi:10.1111/j.0030-1299.2008. 16567.x)
18. Boyer, N., Réale, D., Marmet, J., Pisanu, B. & Chapuis, L. 2010 Personality, space use and tick load in an introduced population of Siberian chipmunks Tanias sibiricus. J. Anim. Ecol. 79, 538-547. (doi:10.1111/j.1365-2656. 2010.01659.x)
19. Brooke, M. D. 1985 The effect of allopreening on tick burdens of molting eudyptid penguins. Auk 102, 893-895.
20. Bush, A. O., Fernández, J. C., Esch, G. W. & Seed, J. R. 2001 Parasitism: the diversity and ecology of animal parasites. Cambridge, UK: Cambridge University Press.
21. Careau, V., Thomas, D., Humphries, M. M. & Réale, D. 2008 Energy metabolism and animal personality. Oikos 117, 641-653. (doi:10.1111/j.0030-1299.2008.16513.x)
22. Clark, C. W. 1994 Antipredator behavior and the asset protection principle. Behav. Ecol. 5, 159-170. (doi:10. 1093/beheco/5.2.159)
23. Coats, J., Poulin, R. & Nakagawa, S. 2010 The consequences of parasitic infections for host behavioural correlations and repeatability. Behaviour 147, 367-382. (doi:10.1163/000579509X12574307194101)
24. Cote, J., Dreiss, A. & Clobert, J. 2008 Social personality trait and fitness. Proc. R. Soc. B. 275, 2851-2858. (doi:10. 1098/rspb.2008.0783)
25. Croft, D. P., Krause, J., Darden, S. K., Ramnarine, I. W., Faria, J. J. & James, R. 2009 Behavioural trait assortment in a social network: patterns and implications. Behav. Ecol. Sociobiol. 63, 1495-1503. (doi:10.1007/s00265- 009-0802-x)
26. Cruz, A. & Wiley, J. W. 1989 The decline of an adaptation in the absence of a presumed selection pressure. Evolution 43, 55-62. (doi:10.2307/2409163)
27. Cruz, A., Prather, J. W., Wiley, J. W. & Weaver, P. F. 2008 Egg rejection behavior in a population exposed to parasitism: Village Weavers on Hispaniola. Behav. Ecol. 19, 398-403. (doi:10.1093/beheco/arm147)
28. Dall, S. R. X., Houston, A. I. & McNamara, J. M. 2004 The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol. Lett. 7, 734-739. (doi:10.1111/j.1461-0248.2004. 00618.x)
29. Dawkins, R. 1982 The extended phenotype. Oxford, UK: Oxford University Press.
30. Dingemanse, N. J. & Réale, D. 2005 Natural selection and animal personality. Behaviour 142, 1159-1184. (doi:10. 1163/156853905774539445)
31. Dingemanse, N. J. & Wolf, M. 2010 Recent models for adaptive personality differences: a review. Phil. Trans. R. Soc. B 365, 3947-3958. (doi:10.1098/rstb.2010.0221)
32. Dingemanse, N. J., Both, C., Drent, P. J. & Tinbergen, J. M. 2004 Fitness consequences of avian personalities in a fluctuating environment. Proc. R. Soc. Lond. B 271, 847-852. (doi:10.1098/rspb.2004.2680)
33. Dingemanse, N. J., Wright, J., Kazem, A. J. N., Thomas, D. K., Hickling, R. & Dawnay, N. 2007 Behavioural syndromes differ predictably between 12 populations of stickleback. J. Anim. Ecol. 76, 1128-1138. (doi:10. 1111/j.1365-2656.2007.01284.x)
34. Dingemanse, N. J., Van der Plas, F., Wright, J., Réale, D., Schrama, M., Roff, D. A., Van der Zee, E. & Barber, I. 2009 Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proc. R. Soc. B 276, 1285-1293. (doi:10.1098/rspb.2008.1555)
35. Dingemanse, N. J., Dochtermann, N. A. & Wright, J. 2010a A method for exploring the structure of behavioural syndromes to allow formal comparison within and between datasets. Anim. Behav. 79, 439-450. (doi:10.1016/j. anbehav. 2009.11.024)
36. Dingemanse, N. J., Kazem, A. J. N., Réale, D. & Wright, J. 2010b Behavioural reaction norms: where animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81-89. (doi:10.1016/j.tree.2009.07.013)
37. Dörücü, M., Adams, C. E., Huntingford, F. A. & Crompton, D. W. T. 1995 How fish-helminth associations arise: an example from Arctic Charr in Loch Rannoch. J. Fish Biol. 47, 1038-1043. (doi:10.1111/j. 1095-8649.1995.tb06027.x)
38. Flegr, J., Havlicek, J., Kodym, P., Maly, M. & Smahel, Z. 2002 Increased risk of traffic accidents in subjects with latent toxoplasmosis: a retrospective case-control study. BMC Infect. Dis. 2, 11. (doi:10.1186/1471- 2334-2-11)
39. Fox, A. & Hudson, P. J. 2001 Parasites reduce territorial behaviour in red grouse (Lagopus lagopus scoticus). Ecol. Lett. 4, 139-143. (doi:10.1046/j.1461-0248.2001.00207.x)
40. Frank, S. A. 1996 Models of parasite virulence. Q. Rev. Biol. 71, 37-78. (doi:10.1086/419267)
41. Fraser, D. F., Gilliam, J. F., Daley, M. J., Le, A. N. & Skalski, G. T. 2001 Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. Am. Nat. 158, 124-135. (doi:10.1086/321307)
42. Gertig, D. M., Kapiga, S. H., Shao, J. F. & Hunter, D. J. 1997 Risk factors for sexually transmitted diseases among women attending family planning clinics in Dar-es-Salaam, Tanzania. Genitourinary Med. 73, 39-43.
43. Giles, N. 1983 Behavioral effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the 3-spined stickleback, Gasterosteus aculeatus L. Anim. Behav. 31, 1192-1194. (doi:10.1016/S0003-3472 (83) 80025-6)
44. Giles, N. 1987 Predation risk and reduced foraging activity in fish-experiments with parasitized and non-parasitized 3-spined sticklebacks, Gasterosteus aculeatus L. J. Fish Biol. 31, 37-44. (doi:10.1111/j.1095-8649. 1987.tb05212.x)
45. Godfrey, S. S., Bull, C. M., James, R. & Murray, K. 2009 Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behav. Ecol. Sociobiol. 63, 1045-1056. (doi:10.1007/s00265- 009-0730-9)
46. Gourbal, B. E. F., Lacroix, A. & Gabrion, C. 2002 Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice. Parasitol. Res. 88, 912-917.
47. Hart, B. L. 1990 Behavioral adaptations to pathogens and parasites-5 strategies. Neurosci. Biobehav. Rev. 14, 273-294. (doi:10.1016/S0149-7634 (05) 80038-7)
48. Hart, B. L. 1992 Behavioral adaptations to parasites-an ethological approach. J. Parasitol. 78, 256-265. (doi:10. 2307/3283472)
49. Hart, B. L. 1997 Behavioural defence. In Host-parasite evolution: general principle and avian models (eds D. H. Clayton & J. Moore), pp. 59-77. Oxford, UK: Oxford University Press.
50. Hechtel, L. J., Johnson, C. L. & Juliano, S. A. 1993 Modification of antipredator behavior of Caecidotea intermedius by its parasite Acanthocephalus dirus. Ecology 74, 710-713. (doi:10.2307/1940798)
51. Helluy, S. & Holmes, J. C. 1990 Serotonin, octopamine, and the clinging behavior induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea). Can. J. Zool. 68, 1214-1220. (doi:10. 1139/z90-181)
52. Houston, A. I. & McNamara, J. M. 1999 Models of adaptive behaviour: an approach based on state. Cambridge, UK: Cambridge University Press.
53. Huffman, M. A. 1997 Current evidence for self-medication in primates: a multidisciplinary perspective. Yearbook Phys. Anthropol. 40, 171-200. (doi:10.1002/(SICI) 1096-8644 (1997))
54. Huntingford, F. A. 1976 Relationship between anti-predator behavior and aggression among conspecifics in 3-spined stickleback, Gasterosteus aculeatus. Anim. Behav. 24, 245-260. (doi:10.1016/S0003-3472 (76) 80034-6)
55. Johnson, J. C. & Sih, A. 2005 Precopulatory sexual cannibalism in fishing spiders (Dolomedes triton): a role for behavioral syndromes. Behav. Ecol. Sociobiol. 58, 390-396. (doi:10.1007/s00265-005-0943-5)
56. Kavaliers, M. & Colwell, D. D. 1995 Decreased predator avoidance in parasitized mice-neuromodulatory correlates. Parasitology 111, 257-263. (doi:10.1017/S0031182000081816)
57. Kavaliers, M., Colwell, D. D. & PerrotSinal, T. S. 1997 Opioid and non-opioid NMDA-mediated predatorinduced analgesia in mice and the effects of parasitic infection. Brain Res. 766, 11-18. (doi:10.1016/S0006-8993 (97) 00521-0)
58. Knudsen, R., Amundsen, P. A. & Klemetsen, A. 2003 Interand intra-morph patterns in helminth communities of sympatric whitefish morphs. J. Fish Biol. 62, 847-859. (doi:10.1046/j.1095-8649.2003.00069.x)
59. Kortet, R., Rantala, M. J. & Hedrick, A. 2007 Boldness in anti-predator behaviour and immune defence in field crickets. Evol. Ecol. Res. 9, 185-197.
60. Krause, J. & Godin, J. G. J. 1994 Influence of parasitism on the shoaling behavior of banded killifish, Fundulus diaphanus. Can. J. Zool. 72, 1775-1779. (doi:10.1139/z94-240)
61. Krause, J., James, R. & Croft, D. P. 2010 Personality in the context of social networks. Phil. Trans. R. Soc. B 365, 4099-4106. (doi:10.1098/rstb. 2010.0216)
62. Kuris, A. M. et al. 2008 Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515-518. (doi:10.1038/nature06970)
63. Lafferty, K. D. 1992 Foraging on prey that are modified by parasites. Am. Nat. 140, 854-867. (doi:10.1086/285444)
64. Lafferty, K. D. 1999 The evolution of trophic transmission. Parasitol. Today 15, 111-115. (doi:10.1016/S0169-4758 (99) 01397-6)
65. Lafferty, K. D. & Kuris, A. M. 1999 How environmental stress affects the impacts of parasites. Limnol. Oceanogr. 44, 925-931. (doi:10.4319/lo.1999. 44.3-part-2.0925)
66. Lafferty, K. D. & Morris, A. K. 1996 Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390-1397. (doi:10. 2307/2265536)
67. Lafferty, K. D., Dobson, A. P. & Kuris, A. M. 2006 Parasites dominate food web links. Proc. Natl Acad. Sci. USA 103, 11211-11216. (doi:10.1073/pnas.0604755103)
68. Lafferty, K. D. et al. 2008 Parasites in food webs: the ultimate missing links. Ecol. Lett. 11, 533-546. (doi:10. 1111/j.1461-0248.2008.01174.x)
69. Lochmillar, R. & Deerenberg, C. 2000 Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98. (doi:10.1034/j.1600-0706.2000.880110.x)
70. MacColl, A. D. C. 2009 Parasite burdens differ between sympatric three-spined stickleback species. Ecography 32, 153-160. (doi:10.1111/j.1600- 0587.2008.05486.x)
71. Madden, J. R., Drewe, J. A., Pearce, G. P. & Clutton-Brock, T. H. 2009 The social network structure of a wild meerkat population: 2. Intragroup interactions. Behav. Ecol. Sociobiol. 64, 81-95. (doi:10.1007/s00265-009-0820-8)
72. Mazzi, D. & Bakker, T. C. M. 2003 A predator's dilemma: prey choice and parasite susceptibility in three-spined sticklebacks. Parasitology 126, 339-347. (doi:10.1017/S0031182003003019)
73. McElreath, R. & Strimling, P. 2006 How noisy information and individual asymmetries can make 'personality' an adaptation: a simple model. Anim. Behav. 72, 1135-1139. (doi:10.1016/j.anbehav. 2006.04.001)
74. McElreath, R., Luttbeg, B., Fogarty, S. P., Brodin, T. & Sih, A. 2007 Evolution of animal personalities. Nature 450, E5-E5. (doi:10.1038/nature06326)
75. Milinski, M. 1985 Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L) under competition for food. Behaviour 93, 203-215. (doi:10.1163/156853986X00883)
76. Moore, J. 2002 Parasites and the behavior of animals. Oxford, UK: Oxford University Press.
77. Mooring, M. S. & Hart, B. L. 1995 Differential grooming rate and tick load of territorial male and female impala Aepyceros melampus. Behav. Ecol. 6, 94-101. (doi:10. 1093/beheco/6.1.94)
78. Morand, S., Manning, S. D. & Woolhouse, M. E. J. 1996 Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proc. R. Soc. Lond. B. 263, 119-128. (doi:10.1098/rspb. 1996.0019)
79. Moskat, C., Szentpeteri, J. & Barta, Z. 2002 Adaptations by great reed warblers brood parasitism: a comparison of populations in sympatry and allopatry with the common cuckoo. Behaviour 139, 1313-1329. (doi:10.1163/ 156853902321104181)
80. Pasternak, A. F., Huntingford, F. A. & Crompton, D. W. T. 1995 Changes in metabolism and behavior of the freshwater copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 110, 395-399. (doi:10.1017/S0031182000064738)
81. Perkins, S. E., Cagnacci, F., Stradiotto, A., Arnoldi, D. & Hudson, P. J. 2009 Comparison of social networks derived from ecological data: implications for inferring infectious disease dynamics. J. Anim. Ecol. 78, 1015-1022. (doi:10.1111/j.1365-2656.2009.01557.x)
82. Petney, T. N. & Andrews, R. H. 1998 Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int. J. Parasitol. 28, 377-393. (doi:10.1016/S0020-7519 (97) 00189-6)
83. Pike, T. W., Samanta, M., Lindstrom, J. & Royle, N. J. 2008 Behavioural phenotype affects social interactions in an animal network. Proc. R. Soc. B 275, 2515-2520. (doi:10.1098/rspb.2008.0744)
84. Plateaux, L. 1972 Sur les modifications produites chez une fourmi par la presence d'un parasite cestode. Ann. Sci. Nat. (Zool.) 14, 203-220.
85. Pontier, D., Fromont, E., Courchamp, F., Artois, M. & Yoccoz, N. G. 1998 Retroviruses and sexual size dimorphism in domestic cats (Felis catus L.). Proc. R. Soc. Lond. B 265, 167-173. (doi:10.1098/rspb. 1998.0278)
86. Poulin, R. 1994 The evolution of parasite manipulation of host behavior-a theoretical analysis. Parasitology 109, S109-S118.
87. Poulin, R. 2007 Evolutionary ecology of parasites. Princeton, NJ: Princeton University Press.
88. 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)
89. Quinn, J. L., Patrick, S. C., Bouwhuis, S., Wilkin, T. A. & Sheldon, B. C. 2009 Heterogeneous selection on a heritable temperament trait in a variable environment. J. Anim. Ecol. 78, 1203-1215. (doi:10.1111/j.1365-2656. 2009.01585.x)
90. Rau, M. E. & Caron, F. R. 1979 Parasite-induced susceptibility of moose to hunting. Can. J. Zool. 57, 2466-2468. (doi:10.1139/z79-321)
91. Read, A. F. 1990 Parasites and the evolution of host sexual behaviour. In Parasitism and host behaviour (eds C. J. Barnard & J. M. Behnke), pp. 117-157. London, UK: Taylor and Francis.
92. Réale, D. & Festa-Bianchet, M. 2003 Predator-induced natural selection on temperament in bighorn ewes. Anim. Behav. 65, 463-470. (doi:10.1006/anbe.2003. 2100)
93. Réale, D., Reader, S. M., Sol, D., McDougall, P. T. & Dingemanse, N. J. 2007 Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291-318. (doi:10.1111/j.1469-185X.2007.00010.x)
94. Reimchen, T. E. 1994 Predators and morphological evolution in threespine stickleback. In Evolutionary biology of the threespine stickleback (eds M. A. Bell & S. A. Foster), pp. 240-273. Oxford, UK: Oxford University Press.
95. Sheldon, B. & Verhulst, S. 1996 Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321. (doi:10.1016/0169-5347 (96) 10039-2)
96. Sih, A., Bell, A. M. & Johnson, J. C. 2004a Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19, 372-378. (doi:10.1016/j.tree. 2004.04.009)
97. Sih, A., Bell, A. M., Johnson, J. C. & Ziemba, R. E. 2004b Behavioral syndromes: an integrative overview. Q. Rev. Biol. 79, 241-277. (doi:10.1086/422893)
98. Sih, A. & Bell, A. M. 2008 Insights for behavioral ecology from behavioral syndromes. Adv. Stud. Behav. 38, 227-281. (doi:10.1016/S0065-3454 (08) 00005-3)
99. Sih, A., Hanser, S. F. & McHugh, K. A. 2009 Social network theory: new insights and issues for behavioral ecologists. Behav. Ecol. Sociobiol. 63, 975-988. (doi:10.1007/s00265-009-0725-6)
100. Smith, B. R. & Blumstein, D. T. 2008 Fitness consequences of personality: a meta-analysis. Behav. Ecol. 19, 448-455. (doi:10.1093/beheco/ arm144)
101. Stamps, J. A. 2007 Growth-mortality tradeoffs and 'personality traits' in animals. Ecol. Lett. 10, 355-363. (doi:10. 1111/j.1461-0248.2007.01034.x)
102. Stirling, D. G., Réale, D. & Roff, D. A. 2002 Selection, structure and the heritability of behaviour. J. Evol. Biol. 15, 277-289. (doi:10.1046/j.1420-9101.2002.00389.x)
103. Tain, L., Perrot-Minnot, M. J. & Cézilly, F. 2006 Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proc. R. Soc. B 273, 3039-3045. (doi:10.1098/rspb.2006.3618)
104. Tain, L., Perrot-Minnot, M. J. & Cézilly, F. 2007 Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species. Biol. Lett. 3, 68-71. (doi:10.1098/rsbl.2006.0583)
105. 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)
106. Tierney, J. F., Huntingford, F. A. & Crompton, D. W. T. 1993 The relationship between infectivity of Schistocephalus solidus (Cestoda) and antipredator behavior of its intermediate host, the 3-spined stickleback, Gasterosteus aculeatus. Anim. Behav. 46, 603-605. (doi:10.1006/anbe.1993.1229)
107. Urdal, K., Tierney, J. F. & Jakobsen, P. J. 1995 The tapeworm Schistocephalus solidus alters the activity and response, but not the predation susceptibility of infected copepods. J. Parasitol. 81, 330-333. (doi:10.2307/3283949)
108. van de Laar, M. J. W., Termorshuizen, F., Slomka, M. J., van Doornum, G. J. J., Ossewaarde, J. M., Brown, D. W. G., Coutinho, R. A. & van den Hoek, J. A. R. 1998 Prevalence and correlates of herpes simplex virus type 2 infection: evaluation of behavioural risk factors. Int. J. Epidemiol. 27, 127-134. (doi:10.1093/ije/27.1.127)
109. van Overveld, T. & Mattysen, E. 2010 Personality predicts spatial responses to food manipulations in free-ranging great tits (Parus major). Biol. Lett. 6, 187-190. (doi:10. 1098/rsbl.2009.0764)
110. Vandeperre, P., Lepolain, B., Carael, M., Nzaramba, D., Zissis, G. & Butzler, J. P. 1987 HIV antibodies in a remote rural area in Rwanda, Central Africa-an analysis of potential risk factors for HIV seropositivity. AIDS 1, 213-215.
111. Vyas, A., Kim, S. K., Giacomini, N., Boothroyd, J. C. & Sapolsky, R. M. 2007 Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl Acad. Sci. USA 104, 6442-6447. (doi:10.1073/pnas.0608310104)
112. Webster, J. P. 1994 The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology 109, 583-589. (doi:10. 1017/S0031182000076460)
113. Webster, J. P., Brunton, C. F. A. & Macdonald, D. W. 1994 Effect of Toxoplasma gondii upon neophobic behavior in wild brown rats Rattus norvegicus. Parasitology 109, 37-43. (doi:10.1017/S003118200007774X)
114. Wedekind, C. & Milinski, M. 1996 Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus? An experimental analysis of behavioural resistance. Parasitology 112, 371-383. (doi:10.1017/S0031182000066609)
115. Wilson, D. S., Coleman, K., Clark, A. B. & Biederman, L. 1993 Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus)-an ecological study of a psychological trait. J. Comp. Psychol. 107, 250-260. (doi:10.1037/0735- 7036.107.3.250)
116. Wolf, M. & Weissing, F. J. 2010 An explanatory framework for adaptive personality differences. Phil. Trans. R. Soc. B 365, 3959-3968. (doi:10.1098/rstb.2010.0215)
117. Wolf, M., van Doorn, G. S., Leimar, O. & Weissing, F. J. 2007 Life-history trade-offs favour the evolution of animal personalities. Nature 447, 581-585. (doi:10. 1038/nature05835)
118. Wolf, M., van Doorn, G. S. & Weissing, F. J. 2008 Evolutionary emergence of responsive and unresponsive personalities. Proc. Natl Acad. Sci. USA 105, 15825-15830. (doi:10.1073/pnas.0805473105)