Genetic and phenotypically flexible components of seasonal variation in immune function

Journal of Experimental Biology

Volumn 217, Issue 9, 2014, Pages 1510-1518

  Versteegh, M A ^a   Helm, B ^b,c   Kleynhans, E J ^a,d   Gwinner, E ^b   Tieleman, B I ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Common garden; Constitutive immunity; Genetic components; Phenotypic flexibility; Seasonal variation; Stonechats

Indexed keywords

ANIMAL; CLIMATE; ESCHERICHIA COLI; GENETICS; IMMUNITY; IMMUNOLOGY; PHENOTYPE; PHYSIOLOGY; POPULATION MIGRATION; SEASON; SONGBIRD; STAPHYLOCOCCUS AUREUS; TEMPERATURE;

ANIMAL MIGRATION; ANIMALS; CLIMATE; ESCHERICHIA COLI; IMMUNITY; PASSERIFORMES; PHENOTYPE; SEASONS; STAPHYLOCOCCUS AUREUS; TEMPERATURE;

EID: 84909992496     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.097105     Document Type: Article

References (67)

1. Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecol. Lett. 9, 467-484.
2. Baldwin, M. W., Winkler, H., Organ, C. L. and Helm, B. (2010). Wing pointedness associated with migratory distance in common-garden and comparative studies of stonechats (Saxicola torquata). J. Evol. Biol. 23, 1050-1063.
3. Bauchinger, U. and Biebach, H. (2006). Transition between moult and migration in a long-distance migratory passerine: Organ flexibility in the African wintering area. J. Ornithol. 147, 266-273.
4. Bauchinger, U., Wohlmann, A. and Biebach, H. (2005). Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia borin). Zoology 108, 97-106.
5. Benson, A.-M. and Winker, K. (2001). Timing of breeding range occupancy among high-latitude passerine migrants. Auk 118, 513-519.
6. Buehler, D. M., Piersma, T., Matson, K. and Tieleman, B. I. (2008). Seasonal redistribution of immune function in a migrant shorebird: Annual-cycle effects override adjustments to thermal regime. Am. Nat. 172, 783-796.
7. Buehler, D. M., Encinas-Viso, F., Petit, M., Vézina, F., Tieleman, B. I. and Piersma, T. (2009a). Limited access to food and physiological trade-offs in a long-distance migrant shorebird. II. Constitutive immune function and the acute-phase response. Physiol. Biochem. Zool. 82, 561-571.
8. Buehler, D. M., Tieleman, B. I. and Piersma, T. (2009b). Age and environment affect constitutive immune function in red knots (Calidris canutus). J. Ornithol. 150, 815-825.
9. Dittami, J. P. and Gwinner, E. (1985). Annual cycles in the African stonechat, Saxicola torquata axillaris, and their relationship to environmental factors. J. Zool. 207, 357-370.
10. Dobryszycka, W. (1997). Biological functions of haptoglobin-new pieces to an old puzzle. Eur. J. Clin. Chem. Clin. Biochem. 35, 647-654.
11. Foster, R. and Kreitzman, L. (2010). Seasons of Life: The Biological Rhythms That Enable Living Things to Thrive and Survive. London: Profile Books.
12. Guernier, V., Hochberg, M. E. and Guégan, J.-F. (2004). Ecology drives the worldwide distribution of human diseases. PLoS Biol. 2, e141.
13. Gwinner, E. (1999). Rigid and flexible adjustments to a periodic environment: Role of circadian and circannual programs. In Proceedings of the 22nd International Ornithological Congress, Durban (ed. N. J. Adams and R. H. Slotow), pp. 2366-2378. Johannesburg: BirdLife South Africa.
14. Gwinner, E., Neusser, V. and Schmidt, E. (1987). Haltung, zucht und eiaufzucht afrikanischer und europäischer schwarzkehlchen Saxicola torquata. Gefederte Welt 111, 118-120, 145-147.
15. Gwinner, E., König, S. and Haley, C. (1995a). Genetic and environmental factors influencing clutch size in equatorial and temperate zone stonechats (Saxicola torquata axillaris and S. t. rubicola): An experimental study. Auk 112, 748-755.
16. Gwinner, E., König, S. and Zeman, M. (1995b). Endogenous gonadal, LH and molt rhythms in tropical stonechats: Effect of pair bond on period, amplitude, and pattern of circannual cycles. J. Comp. Physiol. A 177, 73-79.
17. Hegemann, A., Matson, K. D., Both, C. and Tieleman, B. I. (2012). Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years. Oecologia 170, 605-618.
18. Helm, B. (2009). Geographically distinct reproductive schedules in a changing world: Costly implications in captive stonechats. Integr. Comp. Biol. 49, 563-579.
19. Helm, B., Gwinner, E. and Trost, L. (2005). Flexible seasonal timing and migratory behavior: Results from stonechat breeding programs. Ann. New York Acad. Sci. 1046, 216-227.
20. Helm, B., Schwabl, I. and Gwinner, E. (2009). Circannual basis of geographically distinct bird schedules. J. Exp. Biol. 212, 1259-1269.
21. Illera, J. C., Richardson, D. S., Helm, B., Atienza, J. C. and Emerson, B. C. (2008). Phylogenetic relationships, biogeography and speciation in the avian genus Saxicola. Mol. Phylogenet. Evol. 48, 1145-1154.
22. Janeway, C. A., Travers, P., Walport, M. and Shlomchik, M. J. (2004). Immunobiology: The Immune System in Health and Disease, 6th edn. New York, NY: Garland Publishing.
23. Klaassen, M. (1995). Moult and basal metabolic costs in males of two subspecies of stonechats: The European Saxicola torquata rubicula and the East African S. t. axillaris. Oecologia 104, 424-432.
24. Klasing, K. (2004). The costs of immunity. Acta Zool. Sin. 50, 961-969.
25. König, S. and Gwinner, E. (1995). Frequency and timing of successive broods in captive African and European stonechats Saxicola torquata axillaris and S. t. rubicola. J. Avian Biol. 26, 247-254.
26. Lee, K. A. (2006). Linking immune defenses and life history at the levels of the individual and the species. Integr. Comp. Biol. 46, 1000-1015.
27. Lee, K. A., Wikelski, M., Robinson, W. D., Robinson, T. R. and Klasing, K. C. (2008). Constitutive immune defences correlate with life-history variables in tropical birds. J. Anim. Ecol. 77, 356-363.
28. Ljifeld, J. T., Dunn, P. O. and Whittingham, L. A. (2002). Short-term fluctuations in cellular immunity of tree swallows feeding nestlings. Oecologia 130, 185-190.
29. Lochmiller, R. L., Vestey, M. R. and McMurrey, S. T. (1994). Temporal variation in humoral and cell-mediated immune response in a Sigmodon hispidus population. Ecology 75, 236-245.
30. Lovegrove, B. G. (2003). The influence of climate on the basal metabolic rate of small mammals: A slow-fast metabolic continuum. J. Comp. Physiol. B 173, 87-112.
31. MacDougall-Shackleton, S. A. and Hahn, T. P. (2007). Adaptation and evolution of photoperiod response systems in birds. J. Ornithol. 148 Suppl., 219-224.
32. Machado-Filho, R. A. N., Balsamão, G. M. and Marini, M. A. (2010). Seasonal differences in immune profiles and body conditions of migratory and permanent resident neotropical flycatchers. Condor 112, 579-590.
33. Maizels, R. M. and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: Cellular and molecular mechanisms. Nat. Rev. Immunol. 3, 733-744.
34. Marais, M., Maloney, S. K. and Gray, D. A. (2011). Ambient temperature modulates the magnitude of LPS-induced fevers in Pekin ducks. J. Therm. Biol. 36, 121-127.
35. Martin, L. B. (2005). Trade-offs between molt and immune activity in two populations of house sparrows (Passer domesticus). Can. J. Zool. 83, 780-787.
36. Martin, L. B., Pless, M., Svoboda, J. and Wikelski, M. (2004). Immune activity in temperate and tropical house sparrows: A common-garden experiment. Ecology 85, 2323-2331.
37. Matson, K. D., Ricklefs, R. E. and Klasing, K. C. (2005). A hemolysishemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev. Comp. Immunol. 29, 275-286.
38. Mauck, R. A., Matson, K. D., Philipsborn, J. and Ricklefs, R. E. (2005). Increase in the constitutive innate humoral immune system in Leach's storm-petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate. Funct. Ecol. 19, 1001-1007.
39. Millet, S., Bennett, J., Lee, K. A., Hau, M. and Klasing, K. C. (2007). Quantifying and comparing constitutive immunity across avian species. Dev. Comp. Immunol. 31, 188-201.
40. Møller, A. P. (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.
41. Møller, A. P. and Erritzøe, J. (1998). Host immune defence and migration in birds. Evol. Ecol. 12, 945-953.
42. Moreno-Rueda, G. (2010). Experimental test of a trade-off between moult and immune response in house sparrows Passer domesticus. J. Evol. Biol. 23, 2229-2237.
43. Nelson, R. J., Demas, G. E., Klein, S. L. and Kriegsfeld, L. J. (2002). Seasonal Patterns of Stress, Immune Function and Disease. Cambridge, UK: Cambridge University Press.
44. Newton, I. (2008). The Migration Ecology of Birds. London: Academic Press.
45. Nordling, D., Andersson, M., Zohari, S. and Gustafsson, L. (1998). Reproductive effort reduces specific immune response and parasite resistance. Proc. R. Soc. B 265, 1291-1298.
46. Ochsenbein, A. F. and Zinkernagel, R. M. (2000). Natural antibodies and complement link innate and acquired immunity. Immunol. Today 21, 624-630.
47. Owen, J. C. and Moore, F. R. (2006). Seasonal differences in immunological condition of three species of thrushes. Condor 108, 389-398.
48. Pap, P. L., Vágási, C. I., Tökölyi, J., Czirják, G. A. and Barta, Z. (2010a). Variation in haematological indices and immune function during the annual cycle in the great tit Parus major. Ardea 98, 105-112.
49. Pap, P. L., Czirják, G. A., Vágási, C. I., Barta, Z. and Hasselquist, D. (2010b). Sexual dimorphism in immune function changes during the annual cycle in house sparrows. Naturwissenschaften 97, 891-901.
50. Piersma, T. and Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18, 228-233.
51. Pinheiro, J. and Bates, D. DebRoy, S., Sarkar, D. and R Core Team (2013). Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-105.
52. R Development Core Team (2010). R: A Language and Environment for Statistical Computing. Vienna, Austria: The R Foundation for Statistical Computing.
53. Ricklefs, R. E. and Wikelski, M. (2002). The physiology/life-history nexus. Trends Ecol. Evol. 17, 462-468.
54. Rubenstein, D. R., Parlow, A. F., Hutch, C. R. and Martin, L. B., II (2008). Environmental and hormonal correlates of immune activity in a cooperatively breeding tropical bird. Gen. Comp. Endocrinol. 159, 10-15.
55. Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. B 270, 357-366.
56. Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321.
57. Thiollay, J.-M. (1988). Comparative foraging success of insectivorous birds in tropical and temperate forests: Ecological implications. Oikos 53, 17-30.
58. Tieleman, B. I. (2007). Differences in the physiological responses to temperature among stonechats from three populations reared in a common environment. Comp. Biochem. Physiol. 146A, 194-199.
59. Tieleman, B. I., Williams, J. B., Ricklefs, R. E. and Klasing, K. C. (2005). Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc. R. Soc. B 272, 1715-1720.
60. Tieleman, B. I., Versteegh, M. A., Fries, A., Helm, B., Dingemanse, N. J., Gibbs, H. L. and Williams, J. B. (2009). Genetic modulation of energy metabolism in birds through mitochondrial function. Proc. R. Soc. B 276, 1685-1693.
61. Tieleman, B. I., Croese, E., Helm, B. and Versteegh, M. A. (2010). Repeatability and individual correlates of microbicidal capacity of bird blood. Comp. Biochem. Physiol. 156A, 537-540.
62. Urquhart, E. (2002). Stonechats. A Guide to the Genus Saxicola. London: Christoffer Helm.
63. van de Crommenacker, J., Horrocks, N. P. C., Versteegh, M. A., Komdeur, J., Tieleman, B. I. and Matson, K. D. (2010). Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: Implications for ecologists. J. Exp. Biol. 213, 3527-3535.
64. Versteegh, M. A., Helm, B., Gwinner, E. and Tieleman, B. I. (2012a). Annual cycles of metabolic rate are genetically determined but can be shifted by phenotypic flexibility. J. Exp. Biol. 215, 3459-3466.
65. Versteegh, M. A., Schwabl, I., Jaquier, S. and Tieleman, B. I. (2012b). Do immunological, endocrine and metabolic traits fall on a single pace-of-life axis? Covariation and constraints among physiological systems. J. Evol. Biol. 25, 1864-1876.
66. Williams, T. D. (2012). Hormones, life-history, and phenotypic variation: Opportunities in evolutionary avian endocrinology. Gen. Comp. Endocrinol. 176, 286-295.
67. Zink, R. M., Pavlova, A., Drovetski, S., Wink, M. and Rohwer, S. (2009). Taxonomic status and evolutionary history of the Saxicola torquata complex. Mol. Phylogenet. Evol. 52, 769-773.