An analysis of pre- and post-hatching maternal effects mediated by carotenoids in the blue tit

Journal of Evolutionary Biology

Volumn 20, Issue 1, 2007, Pages 326-339

  Biard, C ^a,c   Surai, P F ^b   Moller A P ^a  

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

^b SCOTTISH AGRICULTURAL COLLEGE   (United Kingdom)

^c UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Antioxidants; Carotenoids; Cell mediated immune response; Cross fostering; Fledgling condition; Maternal effects; Plumage colour

Indexed keywords

ANTIOXIDANT; CAROTENOID; PHYTOHEMAGGLUTININ;

ANTIOXIDANT; CAROTENOID; HATCHING; IMMUNE RESPONSE; LOCAL ADAPTATION; MATERNAL EFFECT; NESTLING; PHENOTYPIC PLASTICITY; REPRODUCTIVE COST; SONGBIRD;

ANIMAL; ARTICLE; BLOOD; CELLULAR IMMUNITY; CHEMISTRY; COMPARATIVE STUDY; FEMALE; FORELIMB; FRANCE; GROWTH, DEVELOPMENT AND AGING; HINDLIMB; HISTOLOGY; IMMUNOLOGY; MATERNAL NUTRITION; METABOLISM; MORPHOMETRICS; NESTING; OOCYTE; PHYSIOLOGY; PIGMENTATION; SONGBIRD;

ANIMALS; ANTIOXIDANTS; BODY WEIGHTS AND MEASURES; CAROTENOIDS; FEMALE; FRANCE; IMMUNITY, CELLULAR; MATERNAL NUTRITION PHYSIOLOGY; NESTING BEHAVIOR; OVUM; PASSERIFORMES; PHYTOHEMAGGLUTININS; PIGMENTATION; TARSUS, ANIMAL; WING;

EID: 33845707836     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2006.01194.x     Document Type: Article

References (80)

1. Bendich, A. 1993. Physiological roles of antioxidants in the immune system. J. Dairy Sci. 76: 2789-2794.
2. Bertram, J.S. & Borthiewicz, H. 1995. Dietary carotenoids inhibit neoplastic transformation and modulate gene expression in mouse and human cells. Am. J. Clin. Nutr. 62: 1327-1336.
3. Biard, C., Surai, P.F. & Møller, A.P. 2005. Effects of carotenoid availability during laying on reproduction in the blue tit. Oecologia 144: 32-44.
4. Biard, C., Surai, P.F. & Møller, A.P. 2006. Carotenoid availability in diet and phenotype of blue and great tit nestlings. J. Exp. Biol. 209: 1004-1015.
5. Blount, J.D., Houston, D.C. & Møller, A.P. 2000. Why egg yolk is yellow. Trends Ecol. Evol. 15: 47-49.
6. 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. Lond. B 269: 29-36.
7. Blount, J.D., Metcalfe, N.B., Arnold, K.E., Surai, P.F., Devevey, G.L. & Monaghan, P. 2003. Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proc. R. Soc. Lond. B 270: 1691-1696.
8. Blount, J.D., Houston, D.C., Surai, P.F. & Møller, A.P. 2004. Egg-laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proc. R. Soc. Lond. B 271 (Suppl.): S79-S81.
9. Bortolotti, G.R., Tella, J.L., Forero, M.G., Dawson, R.D. & Negro, J.J. 2000. Genetics, local environment and health as factors influencing plasma carotenoids in wild American kestrels (Falco sparverius). Proc. R. Soc. Lond. B 267: 1433-1438.
10. Brinkhof, M.W.G., Heeb, P., Kölliker, M. & Richner, H. 1999. Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc. R. Soc. Lond. B 266: 2315-2322.
11. Burnham, K.P. & Anderson, D.R. 1998. Model Selection and Inference: A Practical Information-Theoretic Approach. Springer Verlag, New York.
12. Burri, B.J. 2000. Carotenoids and gene expression. Nutrition 16: 577-578.
13. Chew, B.P. 1993. Role of carotenoids in the immune response. J. Dairy Sci. 76: 2804-2811.
14. Christe, P., Møller, A.P., Saino, N. & de Lope, F. 2000. Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin). Heredity 85: 75-83.
15. Cichoñ, M., Sendecka, J. & Gustafsson, L. 2006. Genetic and environmental variation in immune response of collared flycatcher nestlings. J. Evol. Biol. 19: 1669-1674.
16. Crnokrak, P. & Roff, D.A. 1995. Dominance variance: associations with selection and fitness. Heredity 75: 530-540.
17. Davison, T.F., Morris, T.R. & Payne, L.N. 1996. Poultry Immunology. Carfax Publishing Company, Oxford.
18. Endler, J.A. 1990. On the measurement and classification of colour in studies of animal colour patterns. Biol. J. Linn. Soc. 41: 315-352.
19. Endler, J.A. 2000. Adaptive genetic variation in the wild. In: Adaptive Genetic Variation in the Wild (T. A. Mousseau, B. Sinervo & J. A. Endler, eds), pp. 251-260. Oxford University Press, Oxford.
20. Falconer, D.S., Mackay, T.F.C. 1996. Introduction to Quantitative Genetics, 4th edn. Longman, New York.
21. Fitze, P.S., Kölliker, M. & Richner, H. 2003. Effects of common origin and common environment on nestling plumage coloration in the great tit (Parus major). Evolution 57: 144-150.
22. Freckelton, R.P. 2002. On the misuse of residuals in ecology: regression of residuals vs. multiple regression. J. Anim. Ecol. 71: 542-545.
23. Gebhardt-Heinrich, S.G. & van Noordwijk, A.J. 1991. Nestling growth in the great tit. I. Heritability estimates under different environmental conditions. J. Evol. Biol. 4: 341-362.
24. Goldstein, H. 2003. Multilevel Statistical Models, 3rd edn. Hodder Arnold, London.
25. Goodwin, T.W. 1984. The Biochemistry of Carotenoids. Chapman and Hall, London.
26. Götmark, F. & Ahlström, M. 1997. Parental preference for red mouth of chicks in a songbird. Proc. R. Soc. Lond. B 264: 959-962.
27. Hill, G.E., Inouye, C.Y. & Montgomerie, R. 2002. Dietary carotenoids predict plumage coloration in wild house finches. Proc. R. Soc. Lond. B 269: 1119-1124.
28. Hoffmann, A.A. & Merilä, J. 1999. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14: 96-101.
29. Hõrak, P., Vellau, H., Ots, I. & Møller, A.P. 2000. Growth conditions affect carotenoid-based plumage coloration of great tit nestlings. Naturwissenschaften 87: 460-464.
30. Hõrak, P., Surai, P.F. & Møller, A.P. 2002. Fat-soluble antioxidants in the eggs of great tits Parus major in relation to breeding habitat and laying sequence. Avian Sci. 2: 123-130.
31. Koutsos, E.A., Clifford, A.J., Calvert, C.C. & Klasing, K.C. 2003. Maternal carotenoid status modifies the incorporation of dietary carotenoids into immune tissues of growing chickens (Gallus gallus domesticus). J. Nutr. 133: 1132-1138.
32. Krist, M. & Remeš, V. 2004. Maternal effects and offspring performance: in search of the best method. Oikos 106: 422-426.
33. Kruuk, L.E.B., Merilä, J. & Sheldon, B.C. 2001. Phenotypic selection on a heritable size trait revisited. Am. Nat. 158: 557-571.
34. Kruuk, L.E.B., Slate, J., Pemberton, J.M. & Clutton-Brock, T.H. 2003. Fluctuating asymmetry in a secondary sexual trait: no associations with individual fitness, environmental stress or inbreeding, and no heritability. J. Evol. Biol. 16: 101-113.
35. Lessells, C.M. & Boag, P.T. 1987. Unrepeatable repetabilities: a common mistake. Auk 104: 116-121.
36. Møller, A.P. 1990. Effects of a haematophagous mite on the barn swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution 44: 771-784.
37. Møller, A.P., Biard, C., Blount, J.D., Houston, D.C., Ninni, P., Saino, N. & Surai, P.F. 2000. Carotenoid-dependant signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poultry Biol. Rev. 11: 137-159.
38. McGraw, K.J., Adkins-Regan, E. & Parker, R.S. 2005. Maternally derived carotenoid pigments affect offspring survival, sex-ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92: 375-380.
39. Merilä, J. 1996. Genetic variation in offspring condition: an experiment. Funct. Ecol. 10: 465-474.
40. Merilä, J. 1997. Expression of genetic variation in body size of the collared flycatcher under different environmental conditions. Evolution 51: 526-536.
41. Merilä, J., Przybylo, R. & Sheldon, B.C. 1999. Genetic variation and natural selection on blue tit body condition in different environments. Genet. Res. 73: 165-176.
42. Mousseau, T.A. & Fox, C.W. 1998. Maternal Effects as Adaptations. pp. 375. Oxford University Press, Oxford.
43. Mousseau, T.A. & Roff, D.A. 1987. Natural selection and the heritability of fitness components. Heredity 59: 181-198.
44. Naef-Daenzer, B., Widmer, A. & Nuber, M. 2001. Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J. Anim. Ecol. 70: 730-738.
45. Olson, V.A. & Owens, I.P.F. 1998. Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol. Evol. 13: 510-514.
46. Pakkasmaa, S., Merilä, J. & O'Hara, R.B. 2003. Genetic and maternal effect influences on viability of common frog tadpoles under different environmental conditions. Heredity 91: 117-124.
47. Parmentier, H.K., De Vries Reilingh, G. & Nieuwland, M.G.B. 1998. Kinetic and immunohistochemical characteristics of mitogen-induced cutaneous hypersensitivity in chickens selected for antibody responsiveness. Vet. Immunol. Immunopathol. 66: 367-376.
48. Partali, V., Liaaen-Jensen, S., Slagsvold, T. & Lifjeld, J.T. 1987. Carotenoids in food chain studies. II. The food chain of Parus spp. Monitored by carotenoid analysis. Comp. Biochem. Physiol. B 87: 885-888.
49. Price, T.D. 1998. Maternal and paternal effects in birds. Effects on offspring fitness. In: Maternal Effects as Adaptations (T. A. Mousseau & C. W. Fox, eds), pp. 202-226. Oxford University Press, Oxford.
50. Price, T.D. & Schluter, D. 1991. On the low heritability of life-history traits. Evolution 45: 853-861.
51. Roff, D.A. 1998. The detection and measurement of maternal effects. In: Maternal Effects as Adaptations (T. A. Mousseau & C. W. Fox, eds), pp. 83-96. Oxford University Press, Oxford.
52. Royle, N.J., Surai, P.F. & Hartley, I.R. 2001. Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav. Ecol. 12: 381-385.
53. Royle, N.J., Surai, P.F. & Hartley, I.R. 2003. The effect of variation in dietary intake on maternal deposition of antioxidants in zebra finch eggs. Funct. Ecol. 17: 472-481.
54. Saino, N., Calza, S. & Møller, A.P. 1997. Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J. Anim. Ecol. 66: 827-836.
55. Saino, N., Stradi, R.D., Ninni, P., Pini, E. & Møller, A.P. 1999. Carotenoid plasma concentration, immune profile and plumage ornamentation of male barn swallows (Hirundo rustica). Am. Nat. 154: 441-448.
56. Saino, N., Bertacche, V., Ferrari, R.P., Martinelli, R., Møller, A.P. & Stradi, R.D. 2002. Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc. R. Soc. Lond. B 269: 1729-1733.
57. Saino, N., Ferrari, R.P., 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.
58. Saks, L., McGraw, K.J. & Hõrak, P. 2003a. How feather colour reflect its carotenoid content. Funct. Ecol. 17: 555-561.
59. Saks, L., Ots, I. & Hõrak, P. 2003b. Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134: 301-307.
60. Sharma, J.M. 1990. Avian Cellular Immunology. CRC Press, Boca Raton.
61. Shawkey, M.D. & Hill, G.E. 2005. Carotenoids need structural colours to shine. Biol. Let. 1: 121-124.
62. Slagsvold, T. & Lifjeld, J.T. 1985. Variation in plumage colour of the great tit Parus major in relation to habitat, season and food. J. Zool. 206: 321-328.
63. Smith, H.G. & Wettermark, K.-J. 1995. Heritability of nestling growth in cross-fostered European starlings Sturnus vulgaris. Genetics 141: 657-665.
64. 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.
65. Soler, J.J., Moreno, J. & Potti, J. 2003. Environmental, genetic and maternal components of immunocompetence of nestling pied flycatchers from a cross-fostering study. Evol. Ecol. Res. 5: 259-272.
66. Spilke, J., Piepho, H.P. & Hu, X. 2005. A simulation study on tests of hypotheses and confidence intervals for fixed effects in mixed models for block experiments with missing data. J. Agr. Biol. Envir. St. 10: 374-389.
67. Sturkie, P.D. 1986. Avian Physiology, 4th edn. Springer-Verlag, New York.
68. Surai, P.F. 2000. Effect of selenium and vitamin E content of the maternal diet on the antioxidant system of the yolk and the developing chick. Brit. Poultry Sci. 41: 235-243.
69. Surai, P.F. 2002. Natural Antioxidants in Avian Nutrition and Reproduction. Nottingham university Press, Nottingham, UK.
70. Surai, P.F., Speake, B.K. & Sparks, N.H.C. 2001a. Carotenoids in avian nutrition and embryonic development. 2. Antioxidant properties and discrimination in embryonic tissues. J. Poultry Sci. 38: 117-145.
71. Surai, P.F., Speake, B.K. & Sparks, N.H.C. 2001b. Carotenoids in avian nutrition and embryonic development. 1. Absorption, availability and levels in plasma and egg yolk. J. Poultry Sci. 38: 1-27.
72. Surai, P.F., Speake, B.K., Wood, N.A.R., Blount, J.D., Bortolotti, G.R. & Sparks, N.H.C. 2001c. Carotenoid discrimination by the avian embryo: a lesson from wild birds. Comp. Biochem. Physiol. B 128: 743-750.
73. Svensson, E. & Merilä, J. 1998. Molt and migratory condition in blue tits: a serological study. Condor 98: 825-831.
74. Thessing, A. & Ekman, J. 1994. Selection on the genetical and environmental components of tarsal growth in juvenile willow tits. J. Evol. Biol. 7: 713-726.
75. Tinbergen, J.M. & Boerlijst, M.C. 1990. Nestling weight and survival in individual great tits (Parus major). J. Anim. Ecol. 59: 1113-1127.
76. Tschirren, B., Fitze, P.S. & Richner, H. 2003. Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.). J. Evol. Biol. 16: 91-100.
77. Wade, M.J. 1998. The evolutionary genetics of maternal effects. In: Maternal Effects as Adaptations (T. A. Mousseau & C. W. Fox, eds), pp. 5-21. Oxford University Press, Oxford.
78. Wolf, J.B., Brodie, E.D. III, Cheverud, J.M., Moore, A.J. & Wade, M.J. 1998. Evolutionary consequences of indirect genetic effects. Trends Ecol. Evol. 13: 64-69.
79. Wolf, J.B., Vaughn, T.T., Pletscher, L.S. & Cheverud, J.M. 2002. Contribution of maternal effect QTL to genetic architecture of early growth in mice. Heredity 89: 300-310.
80. Zhang, L.X., Cooney, R.V. & Bertram, J.S. 1992. Carotenoids upregulate connexin 43 gene expression independent of pro-vitamin A or antioxidant properties. Cancer Res. 52: 5707-5712.