Transgenerational immunity in a bird-ectoparasite system: Do maternally transferred antibodies affect parasite fecundity or the offspring's susceptibility to fleas?

Ibis

Volumn 151, Issue 1, 2009, Pages 160-170

  Tschirren, Barbara ^a,b   Siitari, Heli ^c   Saladin, Verena ^b   Richner, Heinz ^b  

^a MACQUARIE UNIVERSITY   (Australia)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF JYVÄSKYLÄ   (Finland)

Author keywords

ELISA; Host parasite interactions; IgG; Immunocompetence; Immunoglobulins; Maternal effects; Parus major

Indexed keywords

ANTIBODY; CAPTIVE POPULATION; ECTOPARASITE; FECUNDITY; FLEA; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNITY; IMMUNOCOMPETENCE; MATERNAL EFFECT; NESTLING; REPRODUCTIVE SUCCESS; VERTICAL TRANSMISSION;

AVES; PARUS MAJOR; SIPHONAPTERA (FLEAS);

EID: 58149096967     PISSN: 00191019     EISSN: 1474919X     Source Type: Journal    
DOI: 10.1111/j.1474-919X.2008.00880.x     Document Type: Article

References (88)

1. Agrawal, A.A., Laforsch, C. Tollrian, R. 1999. Transgenerational induction of defences in animals and plants. Nature 401 : 60 63.
2. Allen, J.R. Nelson, W.A. 1982. Immunological responses to ectoparasites. Fortschr. Zool. 27 : 169 180.
3. Andersson, S., Uller, T., Lõhmus, M. Sundström, F. 2004. Effects of egg yolk testosterone on growth and immunity in a precocial bird. J. Evol. Biol. 17 : 501 505.
4. Apanius, V. 1998. Ontogeny of immune function. In Starck, J.M. Ricklefs, R.E. (eds) Avian Growth and Development: Evolution within the Altricial-Precocial Spectrum : 203 222. Oxford : Oxford University Press.
5. Berthouly, A., Helfenstein, F. Richner, H. 2007. Cellular immune response, stress resistance and competitiveness in nestling Great Tits in relation to maternally transmitted carotenoids. Funct. Ecol. 21 : 335 343.
6. Biard, C., Surai, P.F. Møller, A.P. 2007. An analysis of pre- and post-hatching maternal effects mediated by carotenoids in the Blue Tit. J. Evol. Biol. 20 : 326 339.
7. Bize, P., Roulin, A. Richner, H. 2002. Covariation between egg size and rearing condition determines offspring quality: an experiment with the Alpine Swift. Oecologia 132 : 231 234.
8. Bouslama, Z., Chabi, Y. Lambrechts, M.M. 2001. Chicks resist high parasite intensities in an Algerian population of Blue Tits. Ecoscience 8 : 320 324.
9. Bouslama, Z., Lambrechts, M.M., Ziane, N., Djenidi, R.D. Chabi, Y. 2002. The effect of nest ectoparasites on parental provisioning in a north-African population of the Blue Tit Parus caeruleus. Ibis 144 : E73 E78.
10. Brossard, M. Wikel, S.K. 2004. Tick immunobiology. Parasitology 129 : S161 S176.
11. Buechler, K., Fitze, P.S., Gottstein, B., Jacot, A. Richner, H. 2002. Parasite-induced maternal response in a natural bird population. J. Anim. Ecol. 71 : 247 252.
12. Cheng, S. Lamont, S.J. 1988. Genetic analysis of immunocompetence measures in a White Leghorn Chicken line. Poultry Sci. 67 : 989 995.
13. Christe, P., Richner, H. Oppliger, A. 1996a. Begging, food provisioning, and nestling competition in Great Tit broods infested with ectoparasites. Behav. Ecol. 7 : 127 131.
14. Christe, P., Richner, H. Oppliger, A. 1996b. Of Great Tits and fleas: sleep baby sleep Anim. Behav. 52 : 1087 7092.
15. Christe, P., Møller, A.P. de Lope, F. 1998. Immunocompetence and nestling survival in the House Martin: the tasty chick hypothesis. Oikos 83 : 175 179.
16. Clark, L. Mason, J.R. 1985. Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67 : 169 176.
17. Clark, L. Mason, J.R. 1988. Effect of biologically-active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77 : 174 180.
18. Clayton, D.H. Moore, J. 1997. Host-parasite Evolution. Oxford : Oxford University Press.
19. Fitze, P.S., Clobert, J. Richner, H. 2004a. Long-term life-history consequences of ectoparasite-modulated growth and development. Ecology 85 : 2018-2026.
20. Fitze, P.S., Tschirren, B. Richner, H. 2004b. Life history and fitness consequences of ectoparasites. J. Anim. Ecol. 73 : 216 226.
21. Gasparini, J., McCoy, K.D., Haussy, C., Tveraa, T. Boulinier, T. 2001. Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the Kittiwake Rissa tridactyla. Proc. R. Soc. Lond. B 268 : 647 650.
22. Gasparini, J., McCoy, K.D., Tveraa, T. Boulinier, T. 2002. Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the Kittiwake (Rissa tridactyla). Ecol. Lett. 5 : 519 524.
23. Gasparini, J., McCoy, K.D., Staszewski, V., Haussy, C. Boulinier, T. 2006. Dynamics of anti-Borrelia antibodies in Black-legged Kittiwake (Rissa tridactyla) chicks suggest a maternal educational effect. Can. J. Zool. 84 : 623 627.
24. Goto, N., Kodama, H., Okada, K. Fujimoto, Y. 1978. Suppression of phytohemagglutinin skin response in thymectomised chickens. Poultry Sci. 57 : 246 250.
25. Grindstaff, J.L., Brodie, E.D. III Ketterson, E.D. 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. R. Soc. Lond. B 270 : 2309 2319.
26. Grindstaff, J.L., Hasselquist, D., Nilsson, J.A., Sandell, M., Smith, H.G. Stjernman, M. 2006. Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc. R. Soc. Lond. B 273 : 2551 2557.
27. Groothuis, T.G.G., Eising, C.M., Dijkstra, C. Müller, W. 2005. Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol. Lett. 1 : 78 81.
28. Gwinner, H. Berger, S. 2005. European Starlings: nestling condition, parasites and green nest material during the breeding season. J. Ornithol. 146 : 365 371.
29. Gwinner, H., Oltrogge, M., Trost, L. Nienaber, U. 2000. Green plants in starling nests: effects on nestlings. Anim. Behav. 59 : 301 309.
30. Haywood, S. Perrins, C.M. 1992. Is clutch size in birds affected by environmental conditions during growth? Proc. R. Soc. Lond. B 249 : 195 197.
31. Heeb, P., Werner, I., Kölliker, M. Richner, H. 1998. Benefits of induced host responses against an ectoparasite. Proc. R. Soc. Lond. B 265 : 51 56.
32. Heller, E.D., Leitner, G., Drabkin, N. Melamed, D. 1990. Passive immunization of chicks against Escherichia coli. Avian Pathol. 19 : 345 354.
33. Hõrak, P., Tegelmann, L., Ots, I. Møller, A.P. 1999. Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 121 : 316 322.
34. Hurtrez-Boussès, S., Blondel, J., Perret, P. Renaud, F. 1997a. Relationship between intensity of blowfly infestation and reproductive success in a Corsican population of Blue Tits. J. Avian Biol. 28 : 267 270.
35. Hurtrez-Boussès, S., Perret, P., Renaud, F. Blondel, J. 1997b. High blowfly parasitic loads affect breeding success in a Mediterranean population of Blue Tits. Oecologia 112 : 514 517.
36. Hurtrez-Boussès, S., Blondel, J., Perret, P., Fabreguettes, J. Renaud, F. 1998. Chick parasitism by blowflies affects feeding rates in a Mediterranean population of Blue Tits. Ecol. Lett. 1 : 17 20.
37. Hurtrez-Boussès, S., Renaud, F., Blondel, J., Perret, P. Galan, M.J. 2000. Effects of ectoparasites of young on parents' behaviour in a Mediterranean population of Blue Tits. J. Avian Biol. 31 : 266 269.
38. Johnson, L.S. Albrecht, D.J. 1993. Effects of hematophagous ectoparasites on nestling House Wrens, Troglodytes aedon - who pays the cost of parasitism? Oikos 66 : 255 262.
39. Kennedy, M.W. Nager, R.G. 2006. The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol. Evol. 21 : 653 655.
40. Koutsos, E.A., Lopez, J.C.G. Klasing, K.C. 2007. Maternal and dietary carotenoids interactively affect cutaneous basophil responses in growing chickens (Gallus gallus domesticus). Comp. Biochem. Physiol. B 147 : 87 92.
41. Lawrence, E.C., Arnaudbattandier, F., Grayson, J., Koski, I.R., Dooley, N.J., Muchmore, A.V. Blaese, R.M. 1981. Ontogeny of humoral immune function in normal chickens - a comparison of immunoglobulin-secreting cells in bone-marrow, spleen, lungs and intestine. Clin. Exp. Immunol. 43 : 450 457.
42. Lehmann, T. 1993. Ectoparasites: direct impact on host fitness. Parasitol. Today 9 : 8 13.
43. Lemke, H., Hansen, H. Lange, H. 2003. Non-genetic inheritable potential of maternal antibodies. Vaccine 21 : 3428 3431.
44. Lindén, M., Gustafsson, L. Pärt, T. 1992. Selection on fledging mass in the Collared Flycatcher and the Great Tit. Ecology 73 : 336 343.
45. Lindström, J. 1999. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14 : 343 348.
46. Loye, J.E. Zuk, M. 1991. Bird-Parasite Interactions: Ecology, Evolution and Behaviour. Oxford : Oxford University Press.
47. Martin, L.B., Han, P., Lewittes, J., Kuhlman, J.R., Klasing, K.C. Wikelski, M. 2006. Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct. Ecol. 20 : 290 299.
48. McCorkle, F., Olah, I. Glick, B. 1980. The morphology of the phytohemagglutinin-induced cell response in the chicken's wattle. Poultry Sci. 59 : 616 623.
49. Merino, S. Potti, J. 1995. Pied Flycatchers prefer to nest in clean nest boxes in an area with detrimental nest ectoparasites. Condor 97 : 828 831.
50. Møller, A.P. 1997. Parasitism and the evolution of host life history. In Clayton, D.H. Moore, J. (eds) Host-parasite Evolution: General Principles and Avian Models : 105 127. Oxford : Oxford University Press.
51. Moreno, J., Merino, S., Sanz, J.J., Arriero, E., Morales, J. Tomás, G. 2005. Nestling cell-mediated immune response, body mass and hatching date as predictors of local recruitment in the Pied Flycatcher Ficedula hypoleuca. J. Avian Biol. 36 : 251 260.
52. Müller, W., Groothuis, T.G.G., Kasprzik, A., Dijkstra, C., Alatalo, R.V. Siitari, H. 2005. Prenatal androgen exposure modulates cellular and humoral immune function of Black-headed Gull chicks. Proc. R. Soc. Lond. B 272 : 1971 1977.
53. Müller, W., Deptuch, K., Lopez-Rull, I. Gil, D. 2007. Elevated yolk androgen levels benefit offspring development in a between-clutch context. Behav. Ecol. 18 : 929 936.
54. Oppliger, A., Richner, H. Christe, P. 1994. Effect of an ectoparasite on lay date, nest-site choice, desertation, and hatching success in the Great Tit (Parus major). Behav. Ecol. 5 : 130 134.
55. Owen, J.P. Clayton, D.H. 2006. Where are the parasites in the PHA response? Trends Ecol. Evol. 22 : 228 229.
56. Pihlaja, M., Siitari, H. Alatalo, R.V. 2006. Maternal antibodies in a wild altricial bird: effects on offspring immunity, growth and survival. J. Anim. Ecol. 75 : 1154 1164.
57. Potti, J. 1999. Maternal effects and the pervasive impact of nestling history on egg size in a passerine bird. Evolution 53 : 279 285.
58. Price, P.W. 1980. Evolutionary Biology of Parasites. Princeton : Princeton University Press.
59. Rehmani, S.F. Firdous, S. 1995. Passive-immunity in chicks from a laying flock vaccinated with the Mukteswar strain of Newcastle-Disease virus. Prev. Vet. Med. 23 : 111 118.
60. Reid, J.M., Arcese, P., Keller, L.F. Hasselquist, D. 2006. Long-term maternal effect on offspring immune response in Song Sparrows Melospiza melodia. Biol. Lett. 2 : 573 576.
61. Rendell, W.B. Verbeek, N.A.M. 1996. Old nest material in nest boxes of Tree Swallows: effects on nest-site choice and nest building. Auk 113 : 319 328.
62. Richner, H., Oppliger, A. Christe, P. 1993. Effect of an ectoparasite on reproduction in Great Tits. J. Anim. Ecol. 62 : 703 710.
63. Rubolini, D., Romano, M., Martinelli, R. Saino, N. 2006. Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female Yellow-legged Gull chicks. Behav. Ecol. Sociobiol. 59 : 344 352.
64. Rytkonen, S., Lehtonen, R. Orell, M. 1998. Breeding Great Tits Parus major avoid nestboxes infested with fleas. Ibis 140 : 687 690.
65. Saino, N., Dall'ara, P., Martinelli, R. Møller, A.P. 2002. Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the Barn Swallow. J. Evol. Biol. 15 : 735 743.
66. Saino, N., Ferrari, R., Romano, M., Martinelli, R. Møller, A.P. 2003. Experimental manipulation of egg carotenoids affects immunity of Barn Swallow nestlings. Proc. R. Soc. Lond. B 270 : 2485 2489.
67. SAS Institute 2003. JMP Version 5.1. Cary, NC : SAS Institute Inc.
68. Sinervo, B. 1990. The evolution of maternal investment in lizards - an experimental and comparative-analysis of egg size and its effects on offspring performance. Evolution 44 : 279 294.
69. Smith, N.C., Wallach, M., Petracca, M., Braun, R. Eckert, J. 1994. Maternal transfer of antibodies induced by infection with Eimeria maxima partially protects chickens against challenge with Eimeria tenella. Parasitology 109 : 551 557.
70. Smits, J.E., Bortolotti, G.R. Tella, J.L. 1999. Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct. Ecol. 13 : 567 572.
71. Stanback, M.T. Dervan, A.A. 2001. Within-season nest-site fidelity in Eastern Bluebirds: Disentangling effects of nest success and parasite avoidance. Auk 118 : 743 745.
72. Svensson, L. 1992. Identification Guide to European Passerines. Vitoria : Heraclio Fournier SA.
73. Szép, T. Møller, A.P. 1999. Cost of parasitism and host immune defence in the Sand Martin Riparia riparia: a role for parent-offspring conflict? Oecologia 119 : 9 15.
74. Tella, J.L., Scheuerlein, A. Ricklefs, R.E. 2002. Is cell-mediated immunity related to the evolution of life-history strategies in birds? Proc. R. Soc. Lond. B 269 : 1059 1066.
75. Tripet, F. Richner, H. 1997a. Host responses to ectoparasites: food compensation by parent Blue Tits. Oikos 78 : 557 561.
76. Tripet, F. Richner, H. 1997b. The coevolutionary potential of a 'generalist' parasite, the Hen Flea Ceratophyllus gallinae. Parasitology 115 : 419 427.
77. Tripet, F. Richner, H. 1999a. Dynamics of Hen Flea Ceratophyllus gallinae subpopulations in Blue Tit nests. J. Insect Behav. 12 : 159 174.
78. Tripet, F. Richner, H. 1999b. Density-dependent processes in the population dynamics of a bird ectoparasite Ceratophyllus gallinae. Ecology. 80 : 1267 1272.
79. Tripet, F., Glaser, M. Richner, H. 2002. Behavioural responses to ectoparasites: time-budget adjustments and what matters to Blue Tits Parus caeruleus infested by fleas. Ibis 144 : 461 469.
80. Tschirren, B. Richner, H. 2006. Parasites shape the optimal investment in immunity. Proc. R. Soc. Lond. B 273 : 1773 1777.
81. Tschirren, B., Richner, H. Schwabl, H. 2004. Ectoparasite-modulated deposition of maternal androgens in Great Tit eggs. Proc. R. Soc. Lond. B 271 : 1371 1375.
82. Tschirren, B., Saladin, V., Fitze, P.S., Schwabl, H. Richner, H. 2005. Maternal yolk testosterone does not modulate parasite susceptibility or immune function in Great Tit nestlings. J. Anim. Ecol. 74 : 675 682.
83. Tschirren, B., Bischoff, L.L., Saladin, V. Richner, H. 2007. Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Funct. Ecol. 21 : 372 378.
84. Van Noordwijk, A.J., Van Balen, J.H. Scharloo, W. 1988. Heritability of body size in a natural population of the Great Tit (Parus major) and its relation to age and environmental conditions during growth. Genet. Res. 51 : 149 162.
85. Walker, M., Steiner, S., Brinkhof, M.W.G. Richner, H. 2003. Induced responses of nestling Great Tits reduce Hen Flea reproduction. Oikos 102 : 67 74.
86. Wikel, S.K. 1996. Host immunity to ticks. Annu. Rev. Entomol. 41 : 1 22.
87. Willadsen, P. 1987. Immunological approaches to the control of ticks. Int. J. Parasitol. 17 : 671 677.
88. Wimberger, P.H. 1984. The use of green plant-material in bird nests to avoid ectoparasites. Auk 101 : 615 618.