Eggshell Spottiness Reflects Maternally Transferred Antibodies in Blue Tits

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Holveck, Marie Jeanne ^a,b   Grégoire, Arnaud ^a   Staszewski, Vincent ^a,c   Guerreiro, Romain ^a,d   Perret, Philippe ^a   Boulinier, Thierry ^a   Doutrelant, Claire ^a  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b EARTH AND LIFE INSTITUTE   (Belgium)

^c UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^d UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; IMMUNOGLOBULIN; MATERNAL ANTIBODY;

ANTIBODY TITER; ARTICLE; BIRD; COLORIMETRY; CONTROLLED STUDY; CYANISTES CAERULEUS; EGG LAYING; EGG SHELL; EGG YOLK; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; MALE; MORPHOLOGICAL TRAIT; NONHUMAN; PASSIVE IMMUNIZATION; PHYSICAL CHEMISTRY; PHYSIOLOGICAL STRESS; PIGMENTATION; QUANTITATIVE ANALYSIS; SURFACE PROPERTY;

ANIMALS; ANTIBODIES; CAROTENOIDS; COLOR; EGG SHELL; EGG YOLK; FEMALE; OVUM; PASSERIFORMES; PIGMENTATION; PROTOPORPHYRINS;

AVES; CYANISTES CAERULEUS;

EID: 84870600700     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050389     Document Type: Article

References (61)

1. Moreno J, Osorno JL, (2003) Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecology Letters 6: 803-806.
2. Reynolds SJ, Martin GR, Cassey P, (2009) Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Animal Behaviour 78: 209-215.
3. Cherry MI, Gosler AG, (2010) Avian eggshell coloration: new perspectives on adaptive explanations. Biological Journal of the Linnean Society 100: 753-762.
4. Kennedy GY, Vevers HG, (1976) Survey of avian eggshell pigments. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 55: 117-123.
5. McGraw KJ, (2005) The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Animal Behaviour 69: 757-764.
6. Morales J, Velando A, Moreno J, (2008) Pigment allocation to eggs decreases plasma antioxidants in a songbird. Behavioral Ecology and Sociobiology 63: 227-233.
7. Martínez-de la Puente J, Merino S, Moreno J, Tomas G, Morales J, et al. (2007) Are eggshell spottiness and colour indicators of health and condition in blue tits Cyanistes caeruleus? Journal of Avian Biology 38: 377-384.
8. Baird T, Solomon SE, Tedstone DR, (1975) Localization and characterization of egg-shell porphyrins in several avian species. British Poultry Science 16: 201-&.
9. de Coster G, de Neve L, Lens L, (2012) Intraclutch variation in avian eggshell pigmentation: The anaemia hypothesis. Oecologia 170: 297-304.
10. Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, et al. (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 29-36.
11. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H, (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proceedings of the Royal Society of London Series B-Biological Sciences 266: 1-12.
12. Costantini D, (2010) Complex trade-offs in the pigeon (Columba livia): egg antioxidant capacity and female serum oxidative status in relation to diet quality. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 180: 731-739.
13. Cassey P, Ewen JG, Blackburn TM, Hauber ME, Vorobyev M, et al. (2008) Eggshell colour does not predict measures of maternal investment in eggs of Turdus thrushes. Naturwissenschaften 95: 713-721.
14. Hargitai R, Herényi M, Török J, (2008) Eggshell coloration in relation to male ornamentation, female condition and egg quality in the collared flycatcher Ficedula albicollis. Journal of Avian Biology 39: 413-422.
15. Costantini D, Møller AP, (2008) Carotenoids are minor antioxidants for birds. Functional Ecology 22: 367-370.
16. Faivre B, Grégoire A, Preault M, Cézilly F, Sorci G, (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300: 103.
17. Surai PF, Speake BK, Sparks NHC, (2001) Carotenoids in avian nutrition and embryonic development. 2. Antioxidant properties and discrimination in embryonic tissues. Journal of Poultry Science 38: 117-145.
18. McGraw KJ, Ardia DR, (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. American Naturalist 162: 704-712.
19. Boulinier T, Staszewski V, (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends in Ecology & Evolution 23: 282-288.
20. Morales J, Sanz JJ, Moreno J, (2006) Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biology Letters 2: 334-336.
21. Gosler AG, Connor OR, Bonser RHC, (2011) Protoporphyrin and eggshell strength: Preliminary findings from a passerine bird. Avian Biology Research 4: 214-223.
22. Gosler AG, Higham JP, Reynolds SJ, (2005) Why are birds' eggs speckled? Ecology Letters 8: 1105-1113.
23. García-Navas V, Sanz JJ, Merino S, Martínez-de la Puente J, Lobato E, et al. (2011) Experimental evidence for the role of calcium in eggshell pigmentation pattern and breeding performance in Blue Tits Cyanistes caeruleus. Journal of Ornithology 152: 71-82.
24. Mägi M, Mänd R, Konovalov A, Tilgar V, Reynolds SJ, (2012) Testing the structural-function hypothesis of eggshell maculation in the Great Tit: an experimental approach. Journal of Ornithology 153: 645-652.
25. Afonso S, Vanore G, Batlle A, (1999) Protoporphyrin IX and oxidative stress. Free Radical Research 31: 161-170.
26. Sanz JJ, García-Navas V, (2009) Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus. Journal of Animal Ecology 78: 31-41.
27. Soler JJ, Navarro C, Contreras TP, Avilés JM, Cuervo JJ, (2008) Sexually selected egg coloration in spotless starlings. American Naturalist 171: 183-194.
28. Gosler AG, Barnett PR, Reynolds SJ, (2000) Inheritance and variation in eggshell patterning in the great tit Parus major. Proceedings of the Royal Society of London Series B-Biological Sciences 267: 2469-2473.
29. Westmoreland D, Kiltie RA, (1996) Egg crypsis and clutch survival in three species of blackbirds (Icteridae). Biological Journal of the Linnean Society 58: 159-172.
30. Doutrelant C, Grégoire A, Grnac N, Gomez D, Lambrechts MM, et al. (2008) Female coloration indicates female reproductive capacity in blue tits. Journal of Evolutionary Biology 21: 226-233.
31. Sheldon BC, (2000) Differential allocation: tests, mechanisms and implications. Trends in Ecology & Evolution 15: 397-402.
32. Blondel J, Thomas DW, Charmantier A, Perret P, Bourgault P, et al. (2006) A thirty-year study of phenotypic and genetic variation of blue tits in Mediterranean habitat mosaics. Bioscience 56: 661-673.
33. Holveck MJ, Doutrelant C, Guerreiro R, Perret P, Gomez D, et al. (2010) Can eggs in a cavity be a female secondary sexual signal? Male nest visits and modelling of egg visual discrimination in blue tits. Biology Letters 6: 453-457.
34. Gomez D (2006) AVICOL, a program to analyse spectrometric data. Google website. Available: http://sites.google.com/site/avicolprogram/ or from the author at dodogomezyahoo.fr. Accessed 2012 October 27.
35. McGraw JK, Hill GE (2006) Quantifying colors. In: J. K. McGraw GEH, editor. Bird Coloration: Volume 1, Mechanisms and Measurements. Cambridge, Massachusetts: Harvard University Press.
36. Kadish KM, Smith KM, Guilard R (2000) The prophyrin handbook. London, UK: Academic Press.
37. Lessells CM, Boag PT, (1987) Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
38. Rasband W (2010) ImageJ. 1.38x ed: National Institutes of Health website. Available: http://rsb.info.nih.gov/ij/index.html. Accessed 2012 October 27.
39. Hoyt DF, (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96: 73-77.
40. Montgomerie R (2006) Analyzing colors. In: McGraw GEHKJ, editor. Bird Coloration: Volume 1, Mechanisms and Measurements. Cambridge, Massachusetts: Harvard University Press. pp. 90-147.
41. Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko TS, (2007) Using digital photography to study animal coloration. Biological Journal of the Linnean Society 90: 211-237.
42. Stevens M, Stoddard MC, Higham JP, (2009) Studying primate color: towards visual system-dependent methods. International Journal of Primatology 30: 893-917.
43. R-Development-Core-Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
44. Laucht S, Kempenaers B, Dale J, (2010) Bill color, not badge size, indicates testosterone-related information in house sparrows. Behavioral Ecology and Sociobiology 64: 1461-1471.
45. Gasparini J, McCoy KD, 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. Proceedings of the Royal Society of London Series B-Biological Sciences 268: 647-650.
46. Szigeti B, Török J, Hegyi G, Rosivall B, Hargitai R, et al. (2007) Egg quality and parental ornamentation in the blue tit Parus caeruleus. Journal of Avian Biology 38: 105-112.
47. Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, et al. (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 1729-1733.
48. Groothuis TGG, Eising CM, Blount JD, Surai P, Apanius V, et al. (2006) Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. Journal of Evolutionary Biology 19: 1304-1313.
49. Török J, Hargitai R, Hegyi G, Matus Z, Michl G, et al. (2007) Carotenoids in the egg yolks of collared flycatchers (Ficedula albicollis) in relation to parental quality, environmental factors and laying order. Behavioral Ecology and Sociobiology 61: 541-550.
50. Forstmeier W, Schielzeth H, (2011) Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner's curse. Behavioral Ecology and Sociobiology 65: 47-55.
51. Becker WA (1984) Manual of quantitative genetics. Pullman, Washington: Academic Enterprises.
52. Bulla M, Šálek M, Gosler AG, (2012) Eggshell spotting does not predict male incubation but marks thinner areas of a Shorebird's shells. Auk 129: 26-35.
53. Stevens M, (2011) Avian vision and egg colouration: Concepts and measurements. Avian Biology Research 4: 168-184.
54. Stoddard MC, Fayet AL, Kilner RM, Hinde CA, (2012) Egg speckling patterns do not advertise offspring quality or influence male provisioning in great tits. Plos one 7.
55. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, et al. (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330: 662-665.
56. Christians JK, (2002) Avian egg size: variation within species and inflexibility within individuals. Biological Reviews 77: 1-26.
57. Postma E, van Noordwijk AJ, (2005) Genetic variation for clutch size in natural populations of birds from a reaction norm perspective. Ecology 86: 2344-2357.
58. Senar JC, Figuerola J, Pascual J, (2002) Brighter yellow blue tits make better parents. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 257-261.
59. Merilä J, Fry JD, (1998) Genetic variation and causes of genotype-environment interaction in the body size of blue tit (Parus caeruleus). Genetics 148: 1233-1244.
60. Hargitai R, Prechl J, Török J, (2006) Maternal immunoglobulin concentration in collared flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order. Functional Ecology 20: 829-838.
61. Pahl R, Winkler DW, Graveland J, Batterman BW, (1997) Songbirds do not create long-term stores of calcium in their legs prior to laying: results from high-resolution radiography. Proceedings of the Royal Society of London Series B-Biological Sciences 264: 239-244.