Comparative immunoecology in birds: Hypotheses and tests

Journal of Ornithology

Volumn 148, Issue SUPLL. 2, 2007, Pages

  Hasselquist, Dennis ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Immunocompetence; Latitudinal patterns; Pace of life; Seasonal changes in immunity; Sex dimorphism in immunity

Indexed keywords

ANNUAL CYCLE; BODY SIZE; IMMUNE SYSTEM; PASSERINE; SEASONAL VARIATION; SEXUAL SELECTION;

AVES; PASSERIFORMES;

EID: 36949012272     PISSN: 21937192     EISSN: 21937206     Source Type: Journal    
DOI: 10.1007/s10336-007-0201-x     Document Type: Review

References (88)

1. Alexander J, Stimson WH (1988) Sex hormones and the course of parasitic infection. Parasitol Today 4:1891-1893
2. Anderson RM, May RM (1982) Population biology of infectious diseases. Springer, Berlin Heidelberg New York
3. Ardia D (2005) Tree swallows trade off immune function and reproductive effort differently across their range. Ecology 86:2040-2046
4. Ardia D (2007) The ability to mount multiple immune responses simultaneously varies across the range of the tree swallow. Ecography 30:23-30
5. Bensch S, Stjernman M, Hasselquist D, Östman Ö, Hansson B, Westerdahl H, Torres Pinheiro R (2000) Host specificity and host switching in avian Haematozoa: A study of Plasmodium and Haemoproteus mtDNA amplified from avian blood. Proc R Soc Lond B 267:1583-1589
6. Bensch S, Waldenström J, Jonzén N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112-122
7. Bentley GE, Demas GE, Nelson RJ, Ball GF (1998) Melatonin, immunity and cost of reproduction in European starlings. Proc R Soc Lond B 265:1191-1195
8. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of an immune response. Am Nat 161:367-379
9. Casto JM, Nolan V Jr, Ketterson ED (2001) Steroid hormones and immune function: Experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am Nat 157:408-420
10. Deerenberg C, Apanius V, Daan S, Bos N (1997) Reproductive effort decreases antibody responsiveness. Proc R Soc Lond B 264:1021-1029
11. Duffy DL, Bentley GE, Drazen DL, Ball GF (2000) Effects of testosterone on cell-mediated and humoral immunity in non-breeding European starlings. Behav Ecol 11:654-662
12. Evans MR, Goldsmith AR, Norris SRA (2000) The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 47:156-163
13. Fargallo JA, Laaksonen T, Pöyri V, Korpimäki E (2002) Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecol Lett 5:95-101
14. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603-622
15. Forbes MR (2007) On sex differences in optimal immunity. Trends Ecol Evol 22:111-113
16. Giannessi F, Bianchi F, Dolfi A, Lupetti M (1992) Changes in the chicken bursa of Fabricius and immune response after treatment with melatonin. In Vivo 6:1059-1064
17. Greenman CG, Martin LB, Hau M (2005) Reproductive state, but not testosterone, reduces immune function in male house sparrows (Passer domesticus). Physiol Biochem Zool 78:60-68
18. Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257-261
19. Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnström A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos Trans R Soc B 346:323-331
20. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: A role for parasites. Science 218:384-387
21. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2004) Costs of immunity: Immune responsiveness reduces survival in a vertebrate. Proc R Soc Lond B 271:925-930
22. Hasselquist D, Marsh JA, Sherman PW, Wingfield JC (1999) Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45:167-175
23. Hasselquist D, Watson MF, Winkler DW (2001) Humoral immunocompetence predicts date of egg-laying and reflects female quality in tree swallows. Behav Ecol 12:93-97
24. Hau M (2007) Regulation of male traits by testosterone: Implications for the evolution of vertebrate life histories. Bioessay 29:133-144
25. Haussmann MF, Winkler DW, Huntington CE, Vleck D, Sanneman CE, Hanley D, Vleck CM. (2005) Cell-mediated immunosenescence in birds. Oecologia 145:270-275
26. Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B 267:665-670
27. Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296-299
28. Klasing KC (1998) Nutritional modulation of resistance to infectious diseases. Poult Sci 77:1119-1125
29. Lee KA (2006) Linking immune defense and life history at the level of the individual and the species. Integr Comp Biol 46:1000-1015
30. Lee KA, Martin LB, Hasselquist D, Ricklefs RE, Wikelski M (2006) Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia 150:383-392
31. Lindström KM, Foufopoulos J, Pärn H, Wikelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proc R Soc Lond B 271:1513-1519
32. Martin LB, Pless M, Svoboda J, Wikelski M (2004) Immune activity in temperate and tropical house sparrows: A common-garden experiment. Ecology 85:2323-2331
33. Martin LB, Gilliam J, Han P, Lee K, Wikelski M (2005) Corticosterone suppresses cutaneous immune function in temperate but not tropical house sparrows Passer domesticus. Gen Comp Endocrinol 140:126-135
34. Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006a) Phytohemagglutinin (PHA) induced skin swelling in birds: Histological support for a classic immunoecological technique. Funct Ecol 20:290-299
35. Martin LB, Hasselquist D, Wikelski M (2006b) Immune investments are linked to pace of life in house sparrows. Oecologia 147:565-575
36. Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci USA 98:2071-2076
37. Matson KD, Klasing KC, Ricklefs RE (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Immunol 29:275-286
38. McCorkle F, Olah I, Glick B (1980) Morphology of the phytohemagglutinin-induced cell response in the chickens wattle. Poult Sci 59:616-623
39. McGraw KJ, Ardia DR (2005) Sex differences in carotenoid status and immune performance in zebra finches. Evol Ecol Res 7:251-262
40. Mendes L, Piersma T, Hasselquist D, Matson KD, Ricklefs RE (2006) Variation in the innate and acquired arms of the immune system among five shorebird species. J Exp Biol 209:284-291
41. Millet S, Bennett J, Lee KA, Hau M, Klasing K (2007) Quantifying and comparing constitutive immunity across avian species. Dev Comp Immunol 31:188-201
42. Moore CB, Siopes TD (2002) Effects of lightning conditions and melatonin supplementation on the cellular and humoral immune responses in Japanese quail. Gen Comp Endocrinol 119:95-104
43. Moreno J, Potti J, Yorio P, Borboroglu PG (2001) Sex differences in cell-mediated immunity in the Magellanic penguin Spheniscus magellanicus. Ann Zool Fenn 38:111-116
44. Moreno J, Yorio P, Garcia-Borboroglu P, Potti J, Villar S (2002) Health state and reproductive output in Magellanic penguins (Spheniscus magellanicus). Ethol Ecol Evol 14:19-28
45. Møller AP (1998) Evidence of larger impact of parasites on hosts in the tropics: Investment in immune function within and outside the tropics. Oikos 82:265-270
46. Møller AP, Erritzøe J (1996) Parasite virulence and host immune defense: Host immune response is related to nest re-use in birds. Evolution 50:2066-2072
47. Møller AP, Erritzøe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945-953
48. Møller AP, Erritzøe J, Saino N (2003) Seasonal changes in immune responses and parasite impact on hosts. Am Nat 161:657-671
49. Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511-548
50. Nelson RJ, Demas GE, Klein SL, Kriegsfeld LJ (2002) Seasonal patterns of stress, immune function and disease. Cambridge University Press, Cambridge
51. Norris K, Evans MR (2000) Ecological immunology: Life-history trade-offs and immune defence in birds. Behav Ecol 11:19-26
52. Nowicki S, Peters S, Podos J (1998) Song learning, early nutrition and sexual selection in songbirds. Am Zool 38:179-190
53. Nunn CL (2002) A comparative study of leukocyte counts and disease risk in primates. Evolution 56:177-190
54. Olsen NJ, Kovacs WJ (1996) Gonadal steroids and immunity. Endocr Rev 17:369-384
55. Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Horak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B 268:1175-1181
56. Owen-Ashley NT, Hasselquist D, Wingfield JC (2004) Androgens and the immunocompetence handicap hypothesis: Unravelling direct and indirect pathways of immunosuppression in song sparrows. Am Nat 164:490-505
57. Owen-Ashley NT, Wingfield JC (2006) Seasonal modulation of sickness behaviour in free-living northwestern song sparrows (Melospiza melodia morphna). J Exp Biol 209:3062-3070
58. Palacios MG, Martin TE (2006) Incubation period and immune function: A comparative field study among coexisting birds. Oecologia 146:505-512
59. Peters A (2000) Testosterone treatment is immunosuppressive in superb fairy wrens, yet free-living males with high testosterone are more immunocompetent. Proc R Soc Lond B 267:883-889
60. Piersma T (1997) Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80:623-631
61. Reid J, Arcese P, Keller LF, Elliott KH, Sampson L, Hasselquist D (2007) Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia). Proc R Soc Lond B 274:697-706
62. Richner H, Christe P, Oppliger A (1995) Paternal investment affects prevalence of malaria. Proc Natl Acad Sci USA 92:1192-1194
63. Ricklefs RE (1992) Embryonic-development period and the prevalence of avian blood parasites. Proc Natl Acad Sci USA 89:4722-4725
64. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462-468
65. Rogers D, Randolph SE (2000) The global spread of malaria in a future, warmer world. Science 289:1763-1766
66. Rolff J (2002) Bateman's principle and immunity. Proc R Soc Lond B 269:867-872
67. Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B 265:1637-1641
68. Råberg L, Nilsson JÅ, Ilmonen P, Stjernman M, Hasselquist D (2000) The cost of an immune response: Vaccination reduces parental effort. Ecol Lett 3:382-386
69. Råberg L, Stjernman M, Hasselquist D (2003) Immune responsiveness in adult blue tits: Heritability and effects of nutritional status during ontogeny. Oecologia 136:360-364
70. Sapolsky RM (1992) Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioral endocrinology. MIT Press, Cambridge, pp 287-324
71. Schuurs AHMW, Verheul HAM (1990) Effects of gender and sex steroids on the immune response. J Steroid Biochem 35:157-172
72. Sheldon BC (1993) Sexually transmitted disease in birds: Occurrence and evolutionary significance. Philos Trans R Soc Lond B 339:491-497
73. Sheldon BC, Verhulst S (1996) Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317-321
74. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and radical sexual signals. Proc R Soc Lond B 266:1-12
75. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567-572
76. Stoehr AM, Kokko H (2006) Sexual dimorphism in immunocompetence: What does life-history theory predict? Behav Ecol 17:751-756
77. Svensson E, Råberg L, Koch C, Hasselquist D (1998) Energetic costs of immune responses: Implications for resource allocation and adaptive immunosuppression. Funct Ecol 12:912-919
78. Tella JL, Scheuerlein A, Ricklefs RE (2002) Is cell-mediated immunity related to the evolution of life-history strategies in birds? Proc R Soc Lond B 269:1059-1066
79. Tieleman BI, Williams JB, Ricklefs RE, Klasing KC (2005) Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc R Soc Lond B 272:1715-1720
80. Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U (2002) Cross-species transmission of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545-1554
81. Washburn TC, Medaris DN, Childs B (1965) Sex differences in susceptibility of infections. Pediatrics 35:57-64
82. Westneat DF, Birkhead TR (1998) Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065-1073
83. Zuk M (1990) Reproductive strategies and sex differences in disease susceptibility: An evolutionary viewpoint. Parasitol Today 6:231-233
84. Zuk M (1994) Immunology and the evolution of behavior. In: Real L (ed) Behavioral mechanisms in ecology. Chicago University Press, Chicago, pp 354-368
85. Zuk M (1996) Disease, endocrine-immune interactions, and sexual selection. Ecology 77:1037-1042
86. Zuk M, Johnsen TS (1998) Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc R Soc Lond B 265:1631-1635
87. Zuk M, McKean KA (1996) Sex differences in parasite infections: Patterns and processes. Int J Parasitol 26:1009-1024
88. Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9-S22