Yolk androgens in great tit eggs are related to male attractiveness, breeding density and territory quality

Behavioral Ecology and Sociobiology

Volumn 65, Issue 6, 2011, Pages 1257-1266

  Remeš, Vladimír ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Feather colouration; Maternal effects; Offspring engineering; Paternal effects; Sexual selection

Indexed keywords

AGE CLASS; ANDROGEN; BODY CONDITION; BREEDING SEASON; EGG; FEATHER; FITNESS; HABITAT QUALITY; LAYING DATE; LIFE HISTORY TRAIT; MALE; MATE ATTRACTION; MATERNAL EFFECT; MONOGAMY; ORNAMENTATION; PARENTAL CARE; PHENOTYPIC PLASTICITY; PIGMENT; RESOURCE ALLOCATION; SEXUAL SELECTION; SONGBIRD; TERRITORY;

PARUS MAJOR; PASSERI;

EID: 79956067316     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-011-1139-9     Document Type: Article

References (90)

1. Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol I, Mechanisms and measurements. Harvard University Press, Cambridge, pp 41-89.
2. Andersson S, Uller T, Lõhmus M, Sundström F (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol 17: 501-505.
3. Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc Lond B 364: 1169-1177.
4. Dentressangle F, Boeck L, Torres R (2008) Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, Sula nebouxii. Behav Ecol Sociobiol 62: 1899-1908.
5. Eising CM, Groothuis TGG (2003) The effect of yolk androgens on begging behaviour in black-headed gull chicks. Anim Behav 66: 1027-1034.
6. Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268: 839-846.
7. Eising CM, Müller W, Groothuis TGG (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2: 20-22.
8. Eising CM, Pavlova D, Groothuis TGG, Eens M, Pinxten R (2008) Maternal yolk androgens in European starlings: affected by social environment or individual traits of the mother? Behaviour 145: 51-72.
9. Ferns PN, Hinsley SA (2004) Immaculate tits: head plumage pattern as an indicator of quality in birds. Anim Behav 67: 261-272.
10. Ferns PN, Hinsley SA (2008) Carotenoid plumage hue and chroma signal different aspects of individual and habitat quality in tits. Ibis 150: 152-159.
11. Figuerola J, Senar JC (2000) Measurement of plumage badges: an evaluation of methods used in the great tit Parus major. Ibis 142: 482-484.
12. Garamszegi LZ, Biard C, Eens M, Møller AP, Saino N (2007) Interspecific variation in egg testosterone levels: implications for the evolution of bird song. J Evol Biol 20: 950-965.
13. Garcia-Fernandez V, Guasco B, Tanvez A, Lacroix A, Cucco M, Leboucher G, Malacarne G (2010) Influence of mating preferences on yolk testosterone in the grey partridge. Anim Behav 80: 45-49.
14. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286: 126-128.
15. Gil D, Ninni P, Lacroix A, de Lope F, Tirard C, Marzal A, Møller AP (2006) Yolk androgens in the barn swallow (Hirundo rustica): a test of some adaptive hypotheses. J Evol Biol 19: 123-131.
16. Gil D, Biard C, Larcoix A, Spottiswoode CN, Saino N, Puerta M, Møller AP (2007) Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. Am Nat 169: 802-819.
17. Gilbert L, Rutstein AN, Hazon N, Graves JA (2005) Sex-biased investment in yolk androgens depends on female quality and laying order in zebra finches (Taeniopygia guttata). Naturwissenschaften 92: 178-181.
18. Grindstaff JL, Brodie ED III, Ketterson ED (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transfer. Proc R Soc B 270: 2309-2319.
19. Groothuis TGG, Eising CM, Dijkstra C, Müller W (2005a) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett 1: 78-81.
20. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising CM (2005b) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29: 329-352.
21. Hampl R (1994) Comparison of three immunoassays for testosterone determination. In: Go{double acute}ro{double acute}g S (ed) Advances in steroid analysis '93. Akadémiai Kiadó, Budapest, pp 163-169.
22. Hargitai R, Arnold KE, Herényi M, Prechl J, Török J (2009) Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav Ecol Sociobiol 63: 869-882.
23. Harris WE, Uller T (2009) Reproductive investment when mate quality varies: differential allocation versus reproductive compensation. Philos Trans R Soc Lond B 364: 1039-1048.
24. Hegyi G, Szigeti B, Török J, Eens M (2007) Melanin, carotenoid and structural plumage ornaments: information content and role in great tits Parus major. J Avian Biol 38: 698-708.
25. Hõrak P, Ots I, Vellau H, Spottiswoode C, Møller AP (2001) Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126: 166-173.
26. Isaksson C, Andersson S (2008) Oxidative stress does not influence carotenoid mobilization and plumage pigmentation. Proc R Soc B 275: 309-314.
27. Isaksson C, Uller T, Andersson S (2006) Parental effects on carotenoid-based plumage coloration in nestling great tits, Parus major. Behav Ecol Sociobiol 60: 556-562.
28. Isaksson C, Ornborg J, Prager M, Andersson S (2008) Sex and age differences in reflectance and biochemistry of carotenoid-based colour variation in the great tit Parus major. Biol J Linn Soc 95: 758-765.
29. Johannessen LE, Slagsvold T, Hansen BT, Lifjeld JT (2005) Manipulation of male quality in wild tits: effects on paternity loss. Behav Ecol 16: 747-754.
30. Kawano KM, Yamaguchi N, Kasuya E, Yahara T (2009) Extra-pair mate choice in the female great tit Parus major: good males or compatible males. J Ethol 27: 349-359.
31. Kingma SA, Komdeur J, Vedder O, von Engelhardt N, Korsten P, Groothuis TGG (2009) Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition. Behav Ecol 20: 172-179.
32. Krist M (2010) Egg size and offspring quality: a meta-analysis in birds. Biol Rev. doi: 10. 1111/j. 1469-185X. 2010. 00166. x.
33. Krokene C, Rigstad K, Dale M, Lifjeld JT (1998) The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance. Behav Ecol 9: 649-656.
34. Lemel J, Wallin K (1993) Status signalling, motivational condition and dominance: an experimental study in the great tit, Parus major L. Anim Behav 45: 549-558.
35. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
36. Lessells CM, Dingemanse NJ, Both C (2002) Egg weights, egg component weights, and laying gaps in great tits (Parus major) in relation to ambient temperature. Auk 119: 1091-1103.
37. Loyau A, Saint Jalme M, Mauget R, Sorci G (2007) Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (Pavo cristatus). Behav Ecol Sociobiol 61: 1043-1052.
38. Lubjuhn T, Strohbach S, Brün J, Gerken T, Epplen JT (1999) Extra-pair paternity in great tits (Parus major)-a long term study. Behaviour 136: 1157-1172.
39. Lubjuhn T, Brün J, Gerken T, Epplen JT (2001) Inconsistent pattern of extra-pair paternity in first and second broods of the great tit Parus major. Ardea 89: 69-73.
40. Mänd R, Tilgar V, Møller AP (2005) Negative relationship between plumage colour and breeding output in female great tits, Parus major. Evol Ecol Res 7: 1013-1023.
41. Matysioková B, Remeš V (2010a) Assessing the usefulness of ptilochronology in the study of melanin- and carotenoid-based ornaments in the great tit Parus major. Ibis 152: 397-401.
42. Matysioková B, Remeš V (2010b) Incubation feeding and nest attentiveness in a socially monogamous songbird: role of feather colouration, territory quality and ambient environment. Ethology 116: 596-607.
43. Matysioková B, Remeš V (2010c) Responses to increased costs of activity during incubation in a songbird with female-only incubation: does feather colour signal coping ability? J Ornithol. doi: 10. 1007/s10336-010-0594-9.
44. Mazuc J, Bonneaud C, Chastel O, Sorci G (2003) Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett 6: 1084-1090.
45. Michl G, Török J, Péczely P, Garamszegi LZ, Schwabl H (2005) Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. Behav Ecol 16: 383-388.
46. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11: 137-159.
47. Müller W, Eising CM, Dijkstra C, Groothuis TGG (2002) Sex differences in yolk hormones depend on maternal social status in leghorn chickens (Gallus gallus domesticus). Proc R Soc B 269: 2249-2255.
48. Müller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, Siitari H (2005) Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc R Soc Lond B 272: 1971-1977.
49. Müller W, Vergauwen J, Eens M (2009) Long-lasting consequences of elevated yolk testosterone levels on female reproduction. Behav Ecol Sociobiol 63: 809-816.
50. Müller W, Boonen S, Groothuis TGG, Eens M (2010) Maternal yolk testosterone in canary eggs: toward a better understanding of mechanisms and function. Behav Ecol 21: 493-500.
51. Naef-Daenzer B, Keller LF (1999) The foraging performance of great and blue tits (Parus major and P. caeruleus) in relation to caterpillar development, and its consequences for nestling growth and fledging weight. J Anim Ecol 68: 708-718.
52. Naef-Daenzer B, Widmer F, 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.
53. Navara KJ, Mendonça MT (2008) Yolk androgens as pleiotropic mediators of physiological processes: a mechanistic review. Comp Biochem Physiol A 150: 378-386.
54. Navara KJ, Hill GE, Mendonça MT (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol Biochem Zool 78: 570-578.
55. Navara KJ, Hill GE, Mendonça MT (2006a) Yolk androgen deposition as a compensatory strategy. Behav Ecol Sociobiol 60: 392-398.
56. Navara KJ, Hill GE, Mendonça MT (2006b) Yolk testosterone stimulates growth and immunity in house finch chicks. Physiol Biochem Zool 79: 550-555.
57. Norris KJ (1990) Female choice and the quality of parental care in the great tit Parus major. Behav Ecol Sociobiol 27: 275-281.
58. Norris KJ (1993) Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362: 537-539.
59. Otter KA, Stewart IRK, McGregor PK, Terry AMR, Dabelsteen T, Burke T (2001) Extra-pair paternity among great tits Parus major following manipulation of male signals. J Avian Biol 32: 338-344.
60. Perrins CM (1979) British tits. Collins, London.
61. Pilz KM, Smith HG (2004) Egg yolk androgen levels increase with breeding density in the European starling, Sturnus vulgaris. Funct Ecol 18: 58-66.
62. Pilz KM, Smith HG, Sandell MI, Schwabl H (2003) Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Anim Behav 65: 841-850.
63. Pilz KM, Quiroga M, Schwabl H, Adkins-Regan E (2004) European starling chicks benefit from high yolk testosterone levels during a drought year. Horm Behav 46: 179-192.
64. Pitala N, Ruuskanen S, Laaksonen T, Doligez B, Tschirren B, Gustafsson L (2009) The effects of experimentally manipulated yolk androgens on growth and immune function of male and female nestling collared flycatchers Ficedula albicollis. J Avian Biol 40: 225-230.
65. Quesada J, Senar JC (2006) Comparing plumage colour measurements obtained directly from live birds and from collected feathers: the case of the great tit Parus major. J Avian Biol 37: 609-616.
66. Quesada J, Senar JC (2007) The role of melanin- and carotenoid-based plumage coloration in nest defence in the great tit. Ethology 113: 640-647.
67. Ratikainen II, Kokko H (2010) Differential allocation and compensation: who deserves the silver spoon? Behav Ecol 21: 195-200.
68. Rubolini D, Martinelli R, von Engelhardt N, Romano M, Groothuis TGG, Fasola M, Saino N (2007) Consequences of prenatal androgen exposure for the reproductive performance of female pheasants (Phasianus colchicus). Proc R Soc Lond B 274: 137-142.
69. Ruuskanen S, Doligez B, Tschirren B, Pitala N, Gustafsson L, Groothuis TGG, Laaksonen T (2009) Yolk androgens do not appear to mediate sexual conflict over parental investment in the collared flycatcher Ficedula albicollis. Horm Behav 55: 514-519.
70. Saino N, Ferrari RP, Romano M, Martinelli R, Lacroix A, Gil D, Møller AP (2006) Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters. Behav Ecol 17: 172-181.
71. Safran RJ, Pilz KM, McGraw KJ, Correa SM, Schwabl H (2008) Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behav Ecol Sociobiol 62: 427-438.
72. Safran RJ, McGraw KJ, Pilz KM, Correa SM (2010) Egg-yolk androgen and carotenoid deposition as a function of maternal social environment in barn swallows Hirundo rustica. J Avian Biol 41: 470-478.
73. Sandell MI, Adkins-Regan E, Ketterson ED (2007) Pre-breeding diet affects the allocation of yolk hormones in zebra finches Taeniopygia guttata. J Avian Biol 38: 284-290.
74. Senar JC, Figuerola J, Domènech J (2003) Plumage coloration and nutritional condition in the great tit Parus major: the roles of carotenoids and melanins differ. Naturwissenschaften 90: 234-237.
75. Senar JC, Møller AP, Ruiz I, Negro JJ, Broggi J, Hohtola E (2010) Specific appetite for carotenoids in a colorful bird. PLoS ONE 5: e10716.
76. Sockman KW, Weiss J, Webster MS, Talbott V, Schwabl H (2008) Sex-specific effects of yolk-androgens on growth of nestling American kestrels. Behav Ecol Sociobiol 62: 617-625.
77. Strohbach S, Curio E, Bathen A, Epplen JT, Lubjuhn T (1998) Extrapair paternity in the great tit (Parus major): a test of the "good genes" hypothesis. Behav Ecol 9: 388-396.
78. Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56: 491-497.
79. Svensson L (1992) Identification guide to European passerines, 4th edn. British Trust for Ornithology, London.
80. Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham.
81. Tanvez A, Béguin N, Chastel O, Lacroix A, Leboucher G (2004) Sexually attractive phrases increase yolk androgens deposition in Canaries (Serinus canaria). Gen Comp Endocrinol 138: 113-120.
82. Tanvez A, Parisot M, Chastel O, Leboucher G (2008) Does maternal social hierarchy affect yolk testosterone deposition in domesticated canaries? Anim Behav 75: 929-934.
83. Tobler M, Nilsson JÅ, Nilsson JF (2007) Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol Lett 3: 408-410.
84. Török J, Hargitai R, Hegyi G, Matus Z, Michl G, Péczely P, Rosivall B, Tóth G (2007) Carotenoids in the egg yolks of collared flycatchers (Ficedula albicollis) in relation to parental quality, environmental factors and laying order. Behav Ecol Sociobiol 61: 541-550.
85. Tschirren B, Richner H (2008) Differential effects of yolk hormones on maternal and paternal contribution to parental care. Anim Behav 75: 1989-1994.
86. Tschirren B, Richner H, Schwabl H (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc Lond B 271: 1371-1375.
87. Verboven N, Mateman AC (1997) Low frequency of extra-pair fertilizations in the great tit Parus major revealed by DNA fingerprinting. J Avian Biol 28: 231-239.
88. von Engelhardt N, Carere C, Dijkstra C, Groothuis TGG (2006) Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc Lond B 273: 65-70.
89. Wilkin TA, Garant D, Gosler AG, Sheldon BC (2006) Density effects on life-history traits in a wild population of the great tit Parus major: analyses of long-term data with GIS techniques. J Anim Ecol 75: 604-615.
90. Whittingham LA, Schwabl H (2002) Maternal testosterone in tree swallow eggs varies with female aggression. Anim Behav 63: 63-67.