The evolution of immune defense and song complexity in birds

Evolution

Volumn 57, Issue 4, 2003, Pages 905-912

  Garamszegi, László Zsolt ^a,b   Møller, Anders Pape ^c   Erritzøe, Johannes ^d  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c Laboratoire de Parasitologie Evolutive CNRS UMR 7103 UFR 927   (France)

^d Taps Old Rectory   (Denmark)

Author keywords

Bird song; Bursa of Fabricius; Phytohemagglutinin; Repertoire size; T cell mediated immune response

Indexed keywords

AVIFAUNA; EVOLUTION; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; PARASITE; SEXUAL SELECTION; SONG;

ANIMALIA; AVES; PASSERI; PASSERIFORMES;

EID: 0037719727     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2003.tb00301.x     Document Type: Article

References (65)

1. Arnaiz-Villena, A., M. Álvarez-Tejado, V. Ruíz-del-Valle, C. Garcia-de-la-Torre, P. Varela, M. J. Recio, S. Ferre, and J. Martínez-Laso. 1998. Phylogeny and rapid Northern and Southern hemisphere speciation of goldfinches during the Miocene and Pliocene epochs. Cell. Mol. Life Sci. 54:1031-1041.
2. Balthazart, J. 1983. Hormonal correlates of behavior. Pp. 221-365 in D. S. Farner and J. R. King, eds. Avian biology. Academic Press, New York.
3. Blondel, J., F. Catzeflis, and P. Perret. 1996. Molecular phylogeny and the historical biogeography of the warblers of the genus Sylvia (Aves). J. Evol. Biol. 9:871-891.
4. Brinkhof, M. W. G., P. Heeb, M. Kolliker, and H. Richner. 1999. Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc. R. Soc. Lond. B 266:2315-2322.
5. Buchanan, K. L., C. K. Catchpole, J. W. Lewis, and A. Lodge. 1999. Song as an indicator of parasitism in the sedge warbler. Anim. Behav. 57:307-314.
6. Bull, J. J. 1994. Virulence. Evolution 48:1423-1437.
7. Casto, J. M., V. Nolan, and E. D. Ketterson. 2001. Steroid hormones and immune function: Experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am. Nat. 157:408-420.
8. Catchpole, C. K., and P. J. B. Slater. 1995. Bird song: biological themes and variations. Cambridge Univ. Press, Cambridge, U.K.
9. Cibois, A., and E. Pasquet. 1999. Molecular analysis of the phylogeny of 11 genera of the Corvidea. Ibis 141:297-306.
10. Clayton, D. H. 1991. The influence of parasites on host sexual selection. Parasitol. Today 7:329-334.
11. Côte, I. M., and R. Poulin. 1995. Parasitism and group size in social animals: a meta-analysis. Behav. Ecol. 6:159-165.
12. Cox, F. E. G. 1982. Modern parasitology. Blackwell, Oxford, U.K.
13. Cramp, S., and C. M. Perrins. 1985-1994. The birds of the Western Palearctic. Oxford Univ. Press, Oxford, U.K.
14. Duffy, D. L., and G. F. Ball. 2002. Song predicts immunocompetence in male European starlings (Sturnus vulgaris). Proc. R. Soc. Lond. B 269:847-852.
15. Ewenson, E. L., R. A. Zann, and G. R. Flannery. 2001. Body condition and immune response in wild zebra finches: effects of capture, confinement and captive-rearing. Naturwissenschaften 88:391-394.
16. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.
17. Folstad, I., and A. J. Karter. 1992. Parasites, bright males, and immunocompetence handicap. Am. Nat. 139:603-622.
18. Frank, S. 1996. Models of parasite virulence. Q. Rev. Biol. 71:37-78.
19. Garamszegi, L. Z., A. P. Møller, J. Török, G. Michl, P. Péczely, and M. Richard. 2003. Immune challenge mediates vocal communication in a passerine bird: an experiment. Behav. Ecol. In press.
20. Garland, T. J., A. W. Dickerman, C. M. Janis, and J. A. Jones. 1993. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42:265-292.
21. Gil, D., and M. Gahr. 2002. The honesty of bird song: multiple constraints for multiple traits. Trends Ecol. Evol. 17:133-140.
22. Glick, B. 1983. Bursa of Fabricius. Pp. 443-500 in D. S. Farner and J. R. King, eds. Avian biology. Academic Press, New York.
23. _. 1994. The bursa of Fabricius: the evolution of a discovery. Poult. Sci. 73:979-983.
24. González, G., G. Sorci, A. P. Møller, P. Ninni, C. Haussy, and F. de Lope. 1999. Immunocompetence and condition dependent sexual advertisement in male house sparrows (Passer domesticus). J. Anim. Ecol. 68:1225-1234.
25. Goto, N., H. Kodama, K. Okada, and Y. Fujimoto. 1978. Suppression of phytohaemagglutinin skin response in thymectomized chickens. Poult. Sci. 57:246-250.
26. Grapputo, A., A. Pilastro, A. J. Baker, and G. Martin. 2001. Molecular evidence for phylogenetic relationships among buntings and American sparrows (Emberizidae). J. Avian Biol. 32:95-101.
27. Hamilton, W. D., and M. Zuk. 1982. Heritable true fitness and bright birds: a role for parasites. Science 218:384-387.
28. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford Univ. Press, Oxford, U.K.
29. Hiebert, S. M., P. K. Stoddard, and P. Arcese. 1989. Repertoire size, territory acquisition and reproductive success in the song sparrow. Anim. Behav. 37:266-273.
30. John, J. 1994. The avian spleen: a neglected organ. Q. Rev. Biol. 69:327-351.
31. Krebs, J. R., and D. E. Kroodsma. 1980. Repertoires and geographical variation in birdsong. Adv. Study Behav. 11:143-177.
32. Lochmiller, R. L., M. R. Vestey, and J. C. Boren. 1993. Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503-510.
33. MacDougall-Shackleton, S. A. 1997. Sexual selection and the evolution of song repertoires. Curr. Ornithol. 14:81-124.
34. Martin, T. E., A. P. Møller, S. Merino, and J. Clobert. 2001. Does clutch size evolve in response to parasites and immunocompetence? Proc. Natl. Acad. Sci. USA 98:2071-2076.
35. McCorkle, J. F., I. Olah, and B. Glick. 1980. The morphology of the phytohemagglutinin-induced cell response in the chicken's wattle. Poult. Sci. 59:616-623.
36. Møller, A. P. 1997. Immune defense, extra-pair paternity, and sexual selection in birds. Proc. R. Soc. Lond. B 264:561-566.
37. Møller, A. P., and J. Erritzøe. 1996. Parasite virulence and host immune defense: host immune response is related to nest reuse in birds. Evolution 50:2066-2072.
38. _. 1998. Host immune defense and migration in birds. Evol. Ecol. 12:945-953.
39. _. 2001. Dispersal, vaccination and regression of immune defense organs. Ecol. Lett. 4:484-490.
40. Møller, A. P., G. Sorci, and J. Erritzøe. 1998. Sexual dimorphism in immune defense. Am. Nat. 152:605-619.
41. Møller, A. P., P. Christe, and E. Lux. 1999. Parasitism, host immune function, and sexual selection. Q. Rev. Biol. 74:3-20.
42. Møller, A. P., P.-Y. Henry, and J. Erritzøe. 2000. The evolution of song repertoires and immune defense in birds. Proc. R. Soc. Lond. B 267:165-169.
43. Møller, A. P., S. Merino, C. R. Brown, and R. J. Robertson. 2001. Immune defense and host sociality: a comparative study of swallows and martins. Am. Nat. 158:136-145.
44. Navarro, C., A. Marzal, F. de Lope, and A. P. Møller. 2003. Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos, In press.
45. Noble, E. R., and G. A. Noble. 1976. Parasitology. Lea and Febiger, Philadelphia, PA.
46. Parmentier, H. K., M. B. Kreukniet, B. Goeree, T. F. Davison, S. H. M. Jeurissen, E. G. M.Harmsen, and M. G. B. Nieuwland. 1995. Differences in distribution of lymphocyte antigens in chicken lines divergently selected for antibody responses to sheep red blood cells. Vet. Immunol. Immunopathol. 48:155-168.
47. Poole, A., P. Stettenheim, and F. Gill. 1993-2002. The birds of North America. The American Ornithologists' Union and The Academy of Natural Sciences of Philadelphia, Philadelphia, PA.
48. Read, A. F., and D. M. Weary. 1990. Sexual selection and the evolution of bird song: A test of the Hamilton-Zuk hypothesis. Behav. Ecol. Sociobiol. 26:47-56.
49. _. 1992. The evolution of bird song: comparative analyses. Philos. Trans. R. Soc. Lond. B 338:165-187.
50. Rose, M. E. 1981. Lymphatic system. Pp. 341-384 in A. S. King and J. McLelland, eds. Form and function in birds. Academic Press, London.
51. Saino, N., P. Galeotti, R. Sacchi, and A. P. Møller. 1997a. Song and immunological conditions in male barn swallows (Hirundo rustica). Behav. Ecol. 8:364-371.
52. Saino, N., S. Calza, and A. P. Møller. 1997b. Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J. Anim. Ecol. 66:827-836.
53. Saino, N., S. Calza, and A. P. Møller. 1998. Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos 81:217-228.
54. Searcy, W. A., and M. Andersson. 1986. Sexual selection and the evolution of song. Annu. Rev. Ecol. Syst. 17:507-533.
55. Sheldon, B. C., and S. Verhulst. 1996. Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11:317-321.
56. Sheldon, F. H., B. Slikas, M. Kinnarney, F. B. Gill, E. Zhao, and B. Silverin. 1992. DNA-DNA hybridization evidence of phylogenetic relationships among major lineages of Parus. Auk 109:173-185.
57. Sibley, C. G., and J. E. Ahlquist. 1990. Phylogeny and classification of birds: a study in molecular evolution. Yale Univ. Press, New Haven, CT.
58. Smits, J. E., G. R. Bortolotti, and J. L. Tella. 1999. Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct. Ecol. 13:567-572.
59. Soler, M., M. Martín-Vivaldi, J. M. Marín, and A. P. Møller. 1999. Weight lifting and health status in the black wheatear. Behav. Ecol. 10:281-286.
60. Tella, J. L., A. Scheuerlein, and R. E. Ricklefs. 2002. Is cell-mediated immunity related to the evolution of life-history strategies in birds? Proc. R. Soc. Lond. B 269:1059-1066.
61. Toivanen, P., and A. Toivanen. 1987. Avian immunology: basis and practice. CRC Press, Boca Raton, FL.
62. van Baalen, M. 1998. Coevolution of recovery ability and virulence. Proc. R. Soc. Lond. B 265:317-325.
63. Wakelin, D. 1996. Immunity to parasites. Cambridge Univ. Press, Cambridge, U.K.
64. Weatherhead, P. J., K. J. Metz, G. F. Bennett, and R. E. Irwin. 1993. Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behav. Ecol. Sociobiol. 33:13-23.
65. Wedekind, C., and I. Folstad. 1994. Adaptive or non-adaptive immunosuppression by sex hormones? Am. Nat. 143:936-938.