Maternal transfer of antibodies in vertebrates: Trans-generational effects on offspring immunity

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1513, 2009, Pages 51-60

  Hasselquist, Dennis ^a   Nilsson, Jan Åke ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Epitope blocking; Immune system priming; Maternal antibody transfer; Maternal effects; Offspring growth rate; Trans generational effects

Indexed keywords

ANTIBODY; ANTIGEN; BIRD; DISEASE RESISTANCE; EVOLUTIONARY BIOLOGY; FITNESS; GROWTH RATE; IMMUNE SYSTEM; MATERNAL EFFECT; PATHOGEN; RODENT; YOUNG POPULATION;

ANIMALIA; AVES; RODENTIA; VERTEBRATA;

ANIMAL; ANTIBODY PRODUCTION; BIOLOGICAL MODEL; BIRD; FEMALE; HUMAN; IMMUNOLOGY; OOCYTE; PASSIVE IMMUNIZATION; PREGNANCY; REVIEW; VERTEBRATE;

ANIMALS; ANTIBODY FORMATION; BIRDS; FEMALE; HUMANS; IMMUNITY, MATERNALLY-ACQUIRED; MODELS, IMMUNOLOGICAL; OVUM; PREGNANCY; VERTEBRATES;

EID: 58249086767     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0137     Document Type: Article

References (100)

1. Agrawal, A. A., Laforsch, C. & Tollrian, R. 1999 Transge-nerational induction of defences in animals and plants. Nature 401, 60-63. (doi:10.1038/43425)
2. Albrecht, R., Ennis, F. A., Saltzman, E. J. & Krugman, S. 1977 Persistence of maternal antibody in infants beyond 12 months: mechanism of measles vaccine failure. J. Pediatr. 91, 715-718. (doi:10.1016/S0022-3476(77)81021-4)
3. Anderson, R. W. 1995 On the maternal transmission of immunity: a 'molecular attention' hypothesis. BioSystems 34, 87-105. (doi:10.1016/0303-2647(94)01444-C)
4. Anderson, R. M. & May, R. M. 1982 Population biology of infectious diseases. Berlin, Germany: Springer.
5. Apanius, V. 1998 Ontogeny of immune function. In Avian growth and development: evolution within the altrcial-precocial spectrum (eds J. M. Starck & R. E. Ricklefs), pp. 203-222. Oxford, UK: Oxford University Press.
6. Bernabe, R. R., Couthino, A., Cazenave, P. A. & Forni, L. 1981 Suppression of a 'recurrent' idiotype results in profound alterations of the whole B-cell compartment. Proc. Natl Acad. Sci. USA 78, 6416-6420. (doi:10.1073/pnas.78.10.6416)
7. Biard, C., Surai, P. F. & Møller, A. P. 2007 Analysis of pre-and post-hatching maternal effects mediated by caroten-oids in the blue tit. J. Evol. Biol. 20, 326-333. (doi:10. 1111/j.1420-9101.2006.01194. x)
8. Blount, J. D., Houston, D. C. & Møller, A. P. 2000 Why egg yolk is yellow. Trends Ecol. Evol. 15, 47-49. (doi:10.1016/S0169- 5347 (99)01774-7)
9. Blount, J. D., Surai, P. F., Nager, R. G., Houston, D. C., Møller, A. P., Trewby, M. L. & Kennedy, M. W. 2002 Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc. R. Soc. B 269, 29-36. (doi:10.1098/rspb. 2001.1840)
10. Bly, J. E., Grimm, A. S. & Morris, I. G. 1986 Transfer of passive immunity from mother to young in a teleost fish: haemagglutinating activity in the serum and eggs of plaice, Pleuronectes platessa L. Comp. Biochem. Physiol. A 84, 309-313. (doi:10.1016/0300-9629(86)90620-1)
11. Bonneaud, C., Mazuc, J., Gonzalez, G., Haussy, C., Chastel, O., Faivre, B. & Sorci, G. 2003 Assessing the cost of mounting an immune response. Am. Nat. 161, 367-379. (doi:10.1086/346134)
12. 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. (doi:10.1046/j.1365-2656.2002.00591.x)
13. Carlier, Y. & Truyens, C. 1995 Influence of maternal infection on offspring resistance towards parasites. Parasitai. Today 11, 94-99. (doi: 10.1016/0169-4758(95)80165-0)
14. Cookson, W. O. et al. 1992 Maternal inheritance of atopic IgE responsiveness on chromosome llq. Lancet 340, 381-384. (doi:10.1016/0140-6736(92)91468-N)
15. Daeron, M. 1997 Fc receptor biology. Annu. Rev. Immunol. 15, 203-234. (doi:10.1146/annurev.immunol.15.1.203)
16. Desowitz, R. S. 1971 Plasmodium berghei: enhanced protective immunity after vaccination of white rats of immune mothers. Science 172, 1151-1152. (doi:10.1126/science. 172.3988.1151)
17. Drent, R. H. & Daan, S. 1980 The prudent parent-energetic adjustments in avian breeding. Ardea 68, 225-252.
18. Gasparini, J., McCoy, K. D., Haussy, C., Tveraa, T. & Boulinier, T. 2001 Induced maternal response to the Lyme disease spriochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc. R. Soc. B 268, 647-650. (doi:10.1098/rspb.2000. 1411)
19. 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. (doi:10.1046/j.1461-0248.2002.00345.x)
20. 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. (doi:10.1139/Z06-024)
21. Gasparini, J., Boulinier, T., Gill, V. A., Gil, D., Hatch, S. A. & Roulin, A. 2007 Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird. J. Evol. Biol. 20, 874-880. (doi:10.1111/j.1420-9101.2007.01315.x)
22. Gil, D., Graves, J., Hazon, N. & Wells, A. 1999 Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286, 126-128. (doi:10.1126/science.286.5437.126)
23. Glezen, P. 2003 Effect of maternal antibodies on the infant immune response. Vaccine 21, 3389-3392. (doi:10.1016/S0264-410X(03)00339- 6)
24. Goddard, R. D., Wyeth, P. J. & Varney, W. C. 1994 Vaccination of commercial layer chicks against infectious bursal disease with maternally derived antibodies. Vet. Rec. 135, 273-274.
25. Grindstaff, J. L. 2008 Maternal antibodies reduce costs of an immune response during development. J. Exp. Biol. 211, 654-660. (doi:10.1242/jeb.012344)
26. Grindstaff, J. L., Brodie III, E. D. & Ketterson, E. D. 2003 Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transfer. Proc. R. Soc. B 270, 2309-2319. (doi:10.1098/rspb.2003.2485)
27. Grindstaff, J. L., Demas, G. E. & Ketterson, E. D. 2005 Diet quality affects egg size and number but does not reduce maternal antibody transmission in Japanese quail Coturnix japonica. J. Anim. Ecol. 74, 1051-1058. (doi:10.1111/j.1365-2656.2005.01002.x)
28. Grindstaff, J., Hasselquist, D., Nilsson, J.-Å., Sandell, M., Smith, H. G. & Stjernman, M. 2006 Transge-nerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc. R. Soc. B 273, 2551-2557. (doi:10.1098/rspb.2006.3608)
29. Gustafsson, E., Mattsson, A., Holmdahl, R. & Mattsson, R. 1994 Pregnancy in B-cell-deficient mice: postpartum transfer of immunoglobulins prevents neonatal runting and death. Biol. Reprod. 51, 1173-1180. (doi:10.1095/biolreprod51.6.1173)
30. Haba, S. & Nisonoff, A. 1995 Prolongation of the responsiveness of newborn mice to syngeneic IgE by inhibition of IgE synthesis. Immunol. Lett. 47, 205-208. (doi: 10.1016/0165-2478 (95)00087-3)
31. Hamilton, W. D. & Zuk, M. 1982 Heritable true fitness and bright birds: a role for parasites? Science 218, 384-387. (doi: 10.1126/science.7123238)
32. Hanssen, S. A., Hasselquist, D., Folstad, I. & Erikstad, K. E. 2004 Cost of immunity: immune responsiveness reduces survival in a vertebrate. Proc. R. Soc. B 271, 925-930. (doi: 10.1098/rspb.2004.2678)
33. Hargitai, R., Prechl, J. & Török, J. 2006 Maternal immunoglobulin concentration in collared flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order. Funct. Ecol. 20, 829-838. (doi:10.1111/j.1365-2435.2006.01171.x)
34. Hasselquist, D. 2007 Comparative immunoecology in birds: hypotheses and tests. J. Ornithol. 148(Suppl. 2), S571-S582. (doi: 10.1007/s 10336-007-0201-x)
35. Hasselquist, D. & Nilsson, J.-Å. Submitted. Cost of immune responses: what can we learn from studies of birds?
36. Heeb, P., Werner, L., Kölliker, M. & Richner, H. 1998 Benefits of induced host responses against an ectoparasite. Proc. R. Soc. B 265, 51-56. (doi:10.1098/rspb.1998.0263)
37. Heller, E. D., Leitner, G., Drabkin, N. & Melamed, D. 1990 Passive immunisation of chicks against Escherichia coli. Avian Pathol. 19, 345-354. (doi:10.1080/0307945900 8418685)
38. Heyman, B. 2001 Functions of antibodies in the regulation of B cell responses in vivo. Springer Semin. Immunopathol. 23, 421-432. (doi:10.1007/s281-001-8168-4)
39. Ilmonen, P., Taarna, T. & Hasselquist, D. 2000 Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc. R. Soc. B 267, 665-670. (doi:10.1098/rspb.2000. 1053)
40. Ismail, J., Brait, M., Leo, O. & Urbain, J. 1995 Assessment of a functional role of auto-anti-idiotypes in idiotypic dominance. Eur. J. Immunol. 25, 830-837. (doi:10.1002/eji.1830250330)
41. Janeway, C. A. & Travers, P. 1996 Immunobiology: the immune system in health and disease. London, UK: Current Biology, Ltd.
42. Jarrett, E. E. & Hall, E. 1983 IgE suppression by maternal IgG. Immunology 48, 49-58.
43. Kallio, E. R., Poikonen, A., Vaheri, A., Vapalahti, O., Henttonen, H., Koskela, E. & Mappes, T. 2006 Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proc. R. Soc. B 273, 2771-2776. (doi: 10.1098/rspb.2006.3645)
44. Klasing, K. C. 1998 Nutritional modulation of resistance to infectious diseases. Poult. Sci. 77, 1119-1125.
45. Klasing, K. C. & Leshchinsky, T. V. 1999 Functions, costs, and benefits of the immune system during development and growth. In Proc. 22 Int. Ornithological Cong, (eds N. J. Adams & R. H. Slotow), pp. 2817-2835. Durban, South Africa: BirdLife South Africa.
46. Kowalczyk, K., Daiss, J., Halpern, J. & Roth, T. F. 1985 Quantitation of maternal-fetal IgG transport in the chicken. Immunology 54, 755-762.
47. Kristan, D. M. 2002 Maternal and direct effects of the intestinal nematode Heligmosomoides polygyrus on offspring growth and susceptibility to infection. J. Exp. Biol. 205, 3967-3977. (doi:10.1242/jeb. 012344)
48. Kuby, J. 1992 Immunology. New York, NY: Freeman.
49. Lange, H., Kobarg, J., Yazynin, S., Solterbeck, M., Henningsen, M., Hansen, H. & Lemke, H. 1999 Genetic analysis of the maternally induced affinity enhancement in the non-Oxl idiotypic antibody repertoire of the primary immune response to 2-phenyloxazolone. Scand. J. Immunol. 49, 55-66. (doi:10.1046/j.1365-3083.1999. 00472.x)
50. Lange, H., Kiesch, B., Linden, I., Otto, M., Thierse, H.-J., Shaw, L., Maehnss, K., Hansen, H. & Lemke, H. 2002 Reversal of the adult IgE high responder phenotype in mice by maternally transferred allergen-specific monoclonal IgG antibodies during a sensitive period in early ontogeny. Eur. J. Immunol. 32, 3133-3141. (doi:10.1002/1521-4141 (200211)32:11<3133::AID-IMMU3133> 3. O.CO;2-0)
51. Lawrence, E. C., Arnaud-Battandier, 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.
52. Lemke, H. & Lange, H. 1999 Is there a maternally induced immunological imprinting phase a la Konrad Lorenz? Scand. J. Immunol. 50, 348-354. (doi:10.1046/j.1365-3083.1999.00620.x)
53. Lemke, H. & Lange, H. 2002 Generalization of single immunological experiences by idiotypically mediated clonal connections. Adv. Immunol. 80, 203-241. (doi:10. 1016/S0065-2776(02)80016-5)
54. Lemke, H., Lange, H. & Berek, C. 1994 Maternal immunization modulates the primary immune response to 2-phenyl-oxazolone in BLAB/c mice. Eur. J. Immunol. 24, 3025-3030. (doi:10.1002/eji.1830241216)
55. Lemke, H., Hansen, H. & Lange, H. 2003 Non-genetic inheritable potential of maternal antibodies. Vaccine 21, 3428-3431. (doi:10.1016/S0264-410X(03)00394-3)
56. Lemke, H., Coutinho, A. & Lange, H. 2004 Lamarckian inheritance by somatically acquired maternal IgG pheno-types. Trends Immunol. 25, 180-186. (doi:10.1016/j.it. 2004.02.007)
57. Lochmiller, R. L. & 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)
58. Loye, J. E. & Zuk, M. 1991 Bird - parasite interactions. Oxford, UK: Oxford University Press.
59. Lozano, G. A. & Ydenberg, R. C. 2002 Transgenerational effects of maternal immune challenge in tree swallows (Tachycineta bicolour). Can. J. Zool. 80, 918-925. (doi:10. 1139/z02-063)
60. Lundin, B. S., Dahlman-Höglund, A., Pettersson, I., Dahlgren, U. I. H., Hansson, L. Å. & Telemo, E. 1999 Antibodies given orally in the neonatal period can affect the immune response for two generations: evidence for active maternal influence on the newborn's immune system. Scand. J. Immunol. 50, 651-656. (doi:10.1046/j.1365-3083.1999.00651.x)
61. Mackenzie, N. M. & Keeler, K. D. 1984 A flow microfluori-metric analysis of the binding of immunoglobulins to Fcg receptors of the neonatal mouse jejunal epithelium. Immunology 51, 529-533.
62. Martinez, C., Bernabe, R. R., de la Hera, A., Pereira, P., Cazenave, P. A. & Coutinho, A. 1985 Establishment of idiotypic helper T-cell repertoires early in life. Nature 317, 721-723. (doi:10.1038/317721a0)
63. Möller, A. P. & Erritzoe, J. 1998 Host immune defence and migration in birds. Evol. Ecol. 12, 945-953. (doi:10.1023/A: 1006516222343)
64. Mousseau, T. A. & Fox, C. W. 1998 Maternal effects as adaptations. Oxford, UK: Oxford University Press.
65. Müller, W., Groothius, T. G. G., Dijkstra, C., Siitari, H. & Alatalo, R. 2004 Maternal antibody transmission and breeding densities in the black-headed gull Larus ridibundus. Fund. Ecol. 18, 719-724. (doi:10.1111/j.0269-8463.2004.00902.x)
66. Nicoara, C., Zäch, K., Trachsel, D., Germann, D. & Matter, L. 1999 Decay of passively acquired maternal antibodies against measles, mumps, and rubella viruses. Clin. Diag. Lab. Immunol. 6, 868-871.
67. Nilsson, J.-Å. 2003 Ectoparasitism in marsh tits: costs and functional explanations. Behav. Ecol. 14, 175-181. (doi:10.1093/beheco/14.2.175)
68. Okamoto, Y., Tsutsumi, H., Kumar, N. S. & Ogra, P. L. 1989 Effect of breast feeding on the development of anti-idiotype antibody response to F glycoprotein of respiratory syncytial virus in infant mice after post-partum maternal immunization. J. Immunol. 142, 2507-2512.
69. Ono, Y., Sasaki, T. & Ishida, N. 1974 Regulation of clonal development of immune responding cells by antibody of maternal origin. Nature 250, 593-594. (doi:10.1038/250593a0)
70. 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. (doi: 10.2307/3546640)
71. 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. (doi:10.1111/j.1365-2656.2006.01136. x)
72. Poulin, R. & Thomas, F. 2008 Epigenetic effects of infection on the phenotype of host offspring: parasites reaching across host generations. Oikos 117, 331-335. (doi:10. 1111/j.2007.0030-1299.16435.x)
73. Råberg, L., Nilsson, J.-Å., Ilmonen, P., Stjernman, M. & Hasselquist, D. 2000 The cost of an antibody response: vaccination reduces parental effort. Ecol. Lett. 3, 382-386. (doi:10.1046/j.1461-0248. 2000.00154.x)
74. Råberg, L., Vestberg, M., Hasselquist, D., Holmdahl, R., Svensson, E. & Nilsson, J.-Å. 2002 Basal metabolic rate and the evolution of the adaptive immune system. Proc. R. Soc. B 269, 817-821. (doi:10.1098/rspb.2001.1953)
75. 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. (doi:10.1098/rsbl.2006. 0092)
76. Ricklefs, R. E. & Wikelski, M. 2002 The physiology/life-history nexus. Trends Ecol. Evol. 17, 462-468. (doi:10.1016/S0169-5347(02) 02578-8)
77. Riedler, J. et al. 2001 Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey. Lancet 358, 1129-1133. (doi:10.1016/S0140-6736(01)06252-3)
78. Roberts, S. A. & Turner, M. W. 1983 Specific suppression of rat IgE responses with milk from immunized females and with feeds of serum antibody. Immunology 48, 195-199.
79. Roitt, I., Brostoff, J. & Male, D. K. 1998 Immunology, 5th edn. London, UK: Mosby.
80. Rose, M. E. & Orlans, E. 1981 Immunoglobulins in the egg, embryo, and young chick. Dev. Comp. Immunol. 5, 15-20. (doi:10.1016/S0145- 305X(81)80003-l)
81. Roulin, A. & Heeb, P. 1999 The immunological function of allosuckling. Ecol. Lett. 2, 319-324. (doi:10.1046/j.1461-0248. 1999.00091.x)
82. Rubolini, D., Romano, M., Bonisoli Alquati, A. & Saino, N. 2006 Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull {Larus michahellis) chicks. J. Evol. Biol. 19, 1571-1584. (doi:10.1111/j. 1420-9101. 2006.01121.x)
83. Saino, N., Ferrari, R. P., Martinelli, R., Romano, M., Rubolini, D. & Möller, A. P. 2002a Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc. R. Soc. B 269, 1005-1009. (doi:10. 1098/rspb.2002.1992)
84. Saino, N., Dall'ara, P., Martinelli, R. & Möller, A. P. 2002b Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow. J. Evol. Biol. 15, 735-743. (doi:10.1046/j.1420-9101. 2002.00448.x)
85. Sasaki, T., Ono, Y. & Ishida, N. 1977 Modification of fetal immune system by maternal anti-DNA antibody. I. Enhanced immuneresponse to DNA in the mice exposed to anti-DNA antibody early in life. J. Immunol. 119, 26-30.
86. Schumacher, I. M., Rostal, D. C., Yates, R. A., Brown, D. R., Jacobson, E. R. & Klein, P. A. 1999 Persistence of maternal antibodies against Mycoplasma agassizii in desert tortoise hatchlings. Am. J. Vet. Res. 60, 826-831.
87. Schwabl, H. 1993 Yolk is a source of maternal testosterone for developing birds. Proc. Natl Acad. Sci. USA 90, 11 446-11 450. (doi:10.1073/pnas.90.24.11446)
88. Schwabl, H., Mock, D. W. & Gieg, J. A. 1997 A hormonal mechanism for parental favouritism. Nature 386, 231. (doi: 10.1038/386231a0)
89. Siegrist, C.-A. 2003 Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 21, 3406-3412. (doi:10.1016/S0264-410X(03) 00342-6)
90. Staszewski, V., Gasparini, J., McCoy, K. D., Tveraa, T. & Boulinier, T. 2007a Evidence of an interannual effect of maternal immunization on the immune response of juveniles in a long-lived colonial bird. J. Anim. Ecol. 76, 1215-1223. (doi:10.1111/j.1365-2656.2007.01293.x)
91. Staszewski, V., McCoy, K. D., Tveraa, T. & Boulinier, T. 2007b Interannual dynamics of antibody levels in naturally infected long-lived colonial birds. Ecology 88, 3183-3191. (doi:10.1890/07-0098.1)
92. Stearns, S. C. 1992 The evolution of life histories. Oxford, UK: Oxford University Press.
93. Stern, C. M. 1976 The materno-foetal transfer of carrier protein sensitivity in the mouse. Immunology 30, 443-448.
94. Tollrian, R. & Harwell, C. D. 1999 The ecology and evolution of indudble defenses. Princeton, NJ: Princeton University Press.
95. Valkiūnas, G. 2005 Avian malaria parasites and other Haemosporidia. Boca Raton, FL: CRC Press.
96. Victor, C.j Bona, C. & Pernis, B. 1983 Idiotypes on B lymphocytes: association with immunoglobulins. J. Immunol. 130, 1819-1825.
97. 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. (doi:10.1034/j.1600-0706.2003.12208.x)
98. Williams, T. D., Christians, J. K., Aiken, J. J. & Evanson, M. 1999 Enhanced immune function does not depress reproductive output. Proc. R. Soc. B 266, 753-757. (doi:10.1098/rspb.1999.0701)
99. Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiünas, G. & Bensch, S. 2008 Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Exp. Parasitol. 119, 99-110. (doi:10.1016/j.exppara.2007.12.018)
100. Zuk, M. & Stoehr, A. M. 2002 Immune defense and host life history. Am. Nat. 160, S9-S22. (doi:10.1086/342131)