Darker female pigeons transmit more specific antibodies to their eggs than do paler ones

Biological Journal of the Linnean Society

Volumn 108, Issue 3, 2013, Pages 647-657

  Jacquin, Lisa ^a,b   Haussy, Claudy ^a   Bertin, Claire ^c   Laroucau, Karine ^c   Gasparini, Julien ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^c FRENCH AGENCY FOR FOOD   (France)

Author keywords

Antibody transmission; Chlamydia psittaci; Eumelanin; Humoral immunity; Immune response; KLH; Maternal antibodies; Maternal effects; Plumage coloration

Indexed keywords

ANTIBODY; ANTIGEN; BIRD; EGG; FEMALE; FERAL ORGANISM; IMMUNE SYSTEM; IMMUNITY; MATERNAL EFFECT; PHYSIOLOGICAL RESPONSE; PIGMENT; PLUMAGE;

EID: 84874006877     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/bij.12001     Document Type: Article

References (69)

1. Abdel-Moneim AS, Abdel-Gawad MMA. 2006. Genetic variations in maternal transfer and immune responsiveness to infectious bursal disease virus. Veterinary Microbiology 114: 16-24.
2. Addison B, Ricklefs RE, Klasing KC. 2010. Do maternally derived Ab and early immune experience shape the adult immune response? Functional Ecology 24: 824-829.
3. Aiken L, West S. 1991. Multiple regressions: testing and interpreting interactions. Thousand Oaks, CA: Sage Publications.
4. Andersen AA. 2004. Avian chlamydiosis. In: Commission des normes biologiques & the OIE, ed. Manual of diagnostic tests and vaccines for terrestrial animals. Paris: Office International des Epizooties, 856-867.
5. Bae HD, Kobayashi M, Horio F, Murai A. 2010. Identification of the amino acid residues involved in human IgG transport into egg yolks of Japanese quail (Coturnix japonica). Molecular Immunology 47: 1404-1410.
6. Bize P, Gasparini J, Klopfenstein A, Altwegg R, Roulin A. 2006. Melanin-based coloration is a nondirectionally selected sex-specific signal of offspring development in the alpine swift. Evolution 60: 2370-2380.
7. Boulinier T, Staszewski V. 2008. Maternal transfer of Ab: raising immuno-ecology issues. Trends in Ecology and Evolution 23: 282-288.
8. Burley N. 1977. Parental investment, mate choice and mate quality. Proceedings of the National Academy of Sciences of the United States of America 74: 3476-3479.
9. Collective. 2000. Méthodes d'analyse en santé animale: recherche d'anticorps contre la chlamydiose chez les oiseaux par la technique de fixation du complément. Norme Française AFNOR NF U-47-007.
10. Ducrest A-L, Keller L, Roulin A. 2008. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends in Ecology and Evolution 23: 502-510.
11. Evans KL. 2010. Individual species and urbanisation. In: Gaston KJ, ed. Urban ecology. Cambridge: Cambridge University Press, 53-87.
12. Falconer DS, Mackay TFC. 1996. Introduction to quantitative genetics. Harlow, Essex: Addison Wesley Longman.
13. Fargallo JA, Martinez-Padilla J, Toledano-Diaz A, Santiago-Moreno J, Davila JA. 2007. Sex and testosterone effects on growth, immunity and melanin coloration of nestlings Eurasian kestrels. Journal of Animal Ecology 76: 201-209.
14. Galeotti P, Sacchi R. 2003. Differential parasitaemia in the tawny owl (Strix aluco): effects of color morph and habitat. Journal of Zoology London 261: 91-99.
15. Galvan I, Alonso-Alvarez C. 2008. An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS ONE 3: e3335. doi: 10.1371/journal.pone.0003335.
16. Galvan I, Solano F. 2009. The evolution of eu-and pheomelanic traits may respond to an economy of pigments related to environmental oxidative stress. Pigment Cell Melanoma Research 22: 339-342.
17. Gangoso L, Grande JM, Ducrest A-L, Figuerola J, Bortolotti GR, Andres JA, Roulin A. 2011. MC1R-dependent, melanin-based colour polymorphism is associated with cell-mediated response in the Eleonora's falcon. Journal of Evolutionary Biology 24: 2055-2063.
18. Gasparini J, Bize P, Piault R, Wakamatsu K, Blount J, Ducrest A-L, Roulin A. 2009. Strength and cost of an induced immune response are associated with a heritable melanin-based color trait in female tawny owls. Journal of Animal Ecology 78: 608-616.
19. Gasparini J, Erin N, Bertin C, Jacquin L, Vorimore F, Frantz A, Lenouvel P, Laroucau K. 2011. Impact of urban environment and host phenotype on the epidemiology of Chlamydiaceae in feral pigeons. Environmental Microbiology 13: 3186-3193.
20. Gonzalez G, Sorci G, Moller AP, Ninni P, Haussy C, De Lope F. 1999. Immunocompetence and condition-dependant sexual advertisement in male house sparrows (Passer domesticus). Journal of Animal Ecology 68: 1225-1234.
21. Griggio M, Devigili A, Hoi H, Pilastro A. 2009. Female ornamentation and directional male mate preference in the rock sparrow. Behavioral Ecology 20: 1072-1078.
22. Griggio M, Valera F, Casas A, Pilastro A. 2005. Males prefer ornamented females: a field experiment of male choice in the rock sparrow. Animal Behaviour 69: 1243-1250.
23. Grindstaff JL, Brodie ED III, Ketterson ED. 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal Ab transmission. Proceedings of the Royal Society of London, Series B: Biological Sciences 270: 2309-2319.
24. Haase E, Ito S, Sell A, Wakamatsu K. 1992. Melanin concentrations in feathers from wild and domestic pigeons. Journal of Heredity 83: 64-67.
25. Hanssen S, Bustnesa J, Tveraa T, Hasselquist D, Varepa O, Hendena JA. 2009. Individual quality and reproductive effort mirrored in white wing plumage in both sexes of south polar skuas. Behavioral Ecology 20: 961-966.
26. Hasselquist D, Marsh JA, Sherman PW, Wingfield JC. 1999. Is avian humoral immunocompetence suppressed by testosterone? Behavioral Ecology and Sociobiology 45: 167-175.
27. Hasselquist D, Nilsson JA. 2009. Maternal transfer of Ab in vertebrates: trans-generational effects on offspring immunity. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 364: 51-60.
28. Heeb P, Werner I, Kölliker M, Richner H. 1998. Benefits of induced host responses against an ectoparasite. Proceedings of the Royal Society of London, Series B: Biological Sciences 265: 51-56.
29. Hill GE, McGraw KJ. 2006. Bird coloration. London: Harvard University Press.
30. Hoekstra HE. 2006. Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97: 22-234.
31. Hoi H, Griggio M. 2008. Dual utility of a melanin-based ornament in bearded tits. Ethology 114: 1094-1100.
32. Hubbard JK, Uy AC, Hauber ME, Hoekstra HE, Safran RJ. 2010. Vertebrate pigmentation: from underlying genes to adaptive function. Trends in Genetics 26: 23-239.
33. Jacquin L, Lenouvel P, Haussy C, Ducatez S, Gasparini J. 2011. Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon. Journal of Avian Biology 42: 11-15.
34. Jacquin L, Récapet C, Bouche P, Leboucher G, Gasparini J. 2012. Melanin-based coloration reflects alternative strategies to cope with food limitation in feral pigeons. Behavioral Ecology 23: 907-915.
35. Jawor JM, Breitwisch R. 2003. Melanin ornaments, honesty and sexual selection. The Auk 120: 249-265.
36. Johnston RF, Janiga M. 1995. Feral pigeons. Oxford: Oxford University Press.
37. Johnston RF, Johnson SG. 1989. Non random mating in feral pigeons. The Condor 91: 23-29.
38. Karell P, Ahola K, Karstinen T, Kolunen H, Siitari H, Brommer JE. 2011. Blood parasites mediate morph-specific maintenance costs in a colour polymorphic wild bird. Journal of Evolutionary Biology 24: 1783-1792.
39. Kittilsen S, Johansen IB, Braastad BO, Øverli Ø. 2012. Pigments, parasites and personality: towards a unifying role for steroid hormones? PLoS ONE 7: e34281.
40. Kittilsen S, Schjolden J, Beitnes-Johansen I, Shaw JC, Pottinger TG, Strensen C, Braastad BO, Bakken M, Øverli Ø. 2009. Melanin-based skin spots reflect stress responsiveness in salmonid fish. Hormones and Behavior 56: 292-298.
41. Krüger O, Lindström J. 2001. Lifetime reproductive success in common buzzard, Buteo buteo: from individual variation to population demography. Oikos 93: 260-273.
42. Mafli A, Wakamatsu K, Roulin A. 2011. Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann's tortoises. Animal Behaviour 81: 859-863.
43. Magnino D, Haag-Wackernagel I, Geigenfeind S, Helmecke A, Dovč E, Prukner-Radovčić E, Residbegovićf E, Ilieskig V, Laroucauh K, Donatii M, Martinovj S, Kaletac EF. 2009. Chlamydial infections in feral pigeons in Europe: review of data and focus on public health implications. Veterinary Microbiology 135: 54-67.
44. McGraw KJ. 2007. Dietary mineral content influences melanin-based ornamental coloration. Behavioral Ecology 18: 137-142.
45. McGraw KJ. 2008. An update on the honesty of melanin-based color signals in birds. Pigment Cell Melanoma Research 21: 133-138.
46. McKinnon JS, Pierotti ME. 2010. Colour polymorphism and correlated characters: genetic mechanisms and evolution. Molecular Ecology 19: 5101-5125.
47. Morales J, Moreno J, Merino S, Sanz J, Tomas G, Arriero E, Lobato E, Martinez J. 2007. Female ornaments in the pied flycatcher Ficedula hypoleuca: association with age, health and reproductive success. Ibis 149: 245-254.
48. Moreno J, Møller AP. 2006. Are melanin ornaments signals of antioxidant and immune capacity in birds? Acta Zoologica Sinica 52: 202-208.
49. Mougeot F, Galvan I, Alonso-Alvarez C. 2012. Contrasted effects of an oxidative challenge and α-melanocyte-stimulating hormone on cellular immune responsiveness: an experiment with red-legged partridges Alectoris rufa. Oecologia 169: 385-394.
50. Obukhova NY. 2007. Polymorphism and phene geography of the blue rock pigeon in Europe. Russian Journal of Genetics 43: 492-501.
51. Parejo D, Silva N, Danchin E, Aviles JM. 2011. Informative content of melanin-based colour in adult eurasian kestrels. Journal of Avian Biology 42: 49-60.
52. Parker TH, Stansberry BM, Becker CD, Gipson PS. 2003. Do melanin- or carotenoid-pigmented plumage ornaments signal condition and predict pairing success in the kentucky warbler? The Condor 105: 663-671.
53. Pärn H, Lifjeld JT, Amundsen A. 2005. Female throat ornamentation does not reflect cell-mediated immune response in bluethroats Luscinia s. svecica. Oecologia 146: 496-504.
54. Peig J, Green AJ. 2009. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118: 1883-1891.
55. Piault R, Gasparini J, Bize P, Jenni-Eiermann S, Roulin A. 2009. Pheomelanin-based coloration and the ability to cope with variation in food supply and parasitism. American Naturalist 174: 548-556.
56. Price A, Weadick CJ, Shim J, Rodd FH. 2008. Pigments, patterns, and fish behavior. Zebrafish 5: 297-307.
57. Quesada J, Senar JC. 2009. Cross-fostering experiments to compare carotenoid- and melanin-based plumage traits and long-term parental effects in post-moulted great tits. Behaviour 146: 1235-1251.
58. R Development Core Team. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0. Available at: http://www.R-project.org
59. Rosenblum EB, Hoekstra HE, Nachman MW. 2004. Adaptive reptile color variation and the evolution of the MC1R gene. Evolution 58: 1794-1808.
60. Roulin A. 2004. The evolution, maintenance and adaptive function of genetic color polymorphism in birds. Biological Reviews 9: 815-848.
61. Roulin A, Djikstra C. 2003. Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90: 359-364.
62. Roulin A, Ducrest AL. 2011. Association between melanism, physiology and behavior: a role for the melanocortin system. European Journal of Pharmacology 660: 226-233.
63. Roulin A, Almasi B, Meichtry-Stier KS, Jenni L. 2011. Eumelanin- and pheomelanin-based colour advertise resistance to oxidative stress in opposite ways. Journal of Evolutionary Biology. doi: 10.1111/j.1420-9101.2011.02353.x
64. Roulin A, Jungi TW, Pfister H, Djikstra C. 2000. Female barn owls (Tyto alba) advertise good genes. Proceedings of the Royal Society of London, Series B: Biological Sciences 267: 937-941.
65. Rubenstein DR, Hauber ME. 2008. Dynamic feedback between phenotype and physiology in sexually selected traits. Trends in Ecology and Evolution 23: 655-658.
66. Schmid-Hempel P, Ebert D. 2003. On the evolutionary ecology of specific immune defence. Trends in Ecology and Evolution 18: 27-32.
67. Sirkiä PM, Virolainen M, Laaksonen T. 2010. Melanin has temperature-dependent effects on breeding performance that may maintain phenotypic variation in a passerine bird. Journal of Evolutionary Biology 23: 2385-2396.
68. Tarof SA, Dunn PO, Whittingham LA. 2005. Dual functions of a melanin-based ornament in the common yellowthroat. Proceedings of the Royal Society B 272: 1121-1127.
69. Vergara P, Fargallo JA, Martinez-Padilla J, Lemus JA. 2009. Inter-annual variation and information content of melanin-based coloration in female Eurasian kestrels. Biological Journal of the Linnean Society 97: 781-790.