Behavioral Ecology and Sociobiology

, Volume 67, Issue 3, pp 361–372

Long-lasting effects of yolk androgens on phenotype in the pied flycatcher (Ficedula hypoleuca)

  • Suvi Ruuskanen
  • Esa Lehikoinen
  • Mikko Nikinmaa
  • Heli Siitari
  • Wolfgang Waser
  • Toni Laaksonen
Original Paper


The hormonal environment during early development, such as maternally derived androgens in bird eggs, shapes the development of the offspring in ways that may have important long-term consequences for phenotype and behavior and, ultimately, fitness. We studied the long-term effects of yolk androgens on several phenotypic and physiological traits in male and female pied flycatchers (Ficedula hypoleuca) by experimentally elevating yolk androgen levels and rearing birds in common-garden environment in captivity. We found that high yolk androgen levels increased the basal metabolic rates in both females and males in adulthood. High yolk androgen levels did not affect male melanin coloration or plumage ornaments, or timing or speed of moult in either sex. No effect of androgen treatment on cell-mediated or humoral immune response was found in either sex. Covariation among the measured phenotypic traits was further not altered by androgen treatment. Our results suggest that exposure to high androgen levels can have long-lasting effects on some offspring traits, but do not seem to lead to different phenotypes. Furthermore, the role of yolk androgens affecting sexually selected male traits in our study species seems to be minor. The fitness consequences of yolk androgen-induced higher metabolic rates remain to be studied.


Maternal effect Testosterone Bird Moult Immune defense Basal metabolic rate 


  1. Andersson M (1986) Evolution of condition-dependent sex ornaments and mating preferences—sexual selection based on viability differences. Evolution 40:804–816CrossRefGoogle Scholar
  2. Andersson S, Uller T, Lohmus M, Sundström F (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol 17:501–505PubMedCrossRefGoogle Scholar
  3. Barja G (2007) Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuv Res 10:215–223CrossRefGoogle Scholar
  4. Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105Google Scholar
  5. Bonisoli-Alquati A, Matteo A, Ambrosini R, Rubolini D, Romano M, Caprioli M, Dessi-Fulgheri F, Baratti M, Saino N (2011a) Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Horm Behav 59:75–82PubMedCrossRefGoogle Scholar
  6. Bonisoli-Alquati A, Rubolini D, Caprioli M, Ambrosini R, Romano M, Saino N (2011b) Egg testosterone affects wattle color and trait covariation in the ring-necked pheasant. Behav Ecol Sociobiol 65:1779–1790CrossRefGoogle Scholar
  7. Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc Lond B 268:1337–1344CrossRefGoogle Scholar
  8. Buttemer WA, Warne S, Bech C, Astheimer LB (2008) Testosterone effects on avian basal metabolic rate and aerobic performance: facts and artefacts. Comp Biochem Physiol A 150:204–210CrossRefGoogle Scholar
  9. Carere C, Balthazart J (2007) Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocr Met 18:73–80CrossRefGoogle Scholar
  10. Clotfelter ED, O’Neal DM, Gaudioso JM, Casto JM, Parker-Renga IM, Snajdr EA, Duffy DL, Nolan V, Ketterson ED (2004) Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Horm Behav 46:171–178PubMedCrossRefGoogle Scholar
  11. Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251PubMedGoogle Scholar
  12. Cucco M, Guasco B, Malacarne G, Ottonelli R, Tanvez A (2008) Yolk testosterone levels and dietary carotenoids influence growth and immunity of grey partridge chicks. Gen Comp Endocr 156:418–425PubMedCrossRefGoogle Scholar
  13. Drost R (1936) Über das Brutkleid männlicher Trauerfliegenfänger, Muscicapa hypoleuca (Pall.). Vogelzug 6:179–186Google Scholar
  14. Dufty AM, Clobert J, Møller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196CrossRefGoogle Scholar
  15. Duttmann H, Dieleman S, Groothuis TGG (1999) Timing of moult in male and female shelducks Tadorna tadorna: effects of androgens and mates. Ardea 87:33–39Google Scholar
  16. Eaton MD, Lanyon SM (2003) The ubiquity of avian ultraviolet plumage reflectance. Proc R Soc Lond B 270:1721–1726CrossRefGoogle Scholar
  17. Eeva T, Hasselquist D, Tummeleht L, Nikinmaa M, Ilmonen P (2005) Pollution related effects on immune function and stress in a free-living population of pied flycatcher Ficedula hypoleuca. J Avian Biol 36:405–412CrossRefGoogle Scholar
  18. Eising CM, Visser GH, Müller W, Groothuis TGG (2003) Steroids for free? No metabolic costs of elevated maternal androgen levels in the black-headed gull. J Exp Biol 206:3211–3218PubMedCrossRefGoogle Scholar
  19. Eising CM, Müller W, Groothuis TGG (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2:20–22PubMedCrossRefGoogle Scholar
  20. Forslund P, Pärt T (1995) Age and reproduction in birds—hypotheses and tests. Trends Ecol Evol 10:374–378PubMedCrossRefGoogle Scholar
  21. Galloway LF (2005) Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytol 166:93–99PubMedCrossRefGoogle Scholar
  22. Gil D (2008) Hormones in avian eggs: physiology, ecology and behavior. Adv Stud Behav 38:337–398Google Scholar
  23. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  24. Gil D, Ninni P, Lacroix A, De Lope F, Tirard C, Marzal A, Moller AP (2006) Yolk androgens in the barn swallow (Hirundo rustica): a test of some adaptive hypotheses. J Evol Biol 19:123–131PubMedCrossRefGoogle Scholar
  25. Ginn HB, Melville DS (1983) Moult in birds. British Trust for Ornithology, TringGoogle Scholar
  26. Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos T Roy Soc B 363:1647–1661CrossRefGoogle Scholar
  27. Groothuis TGG, von Engelhardt N (2005) Investigating maternal hormones in avian eggs: measurement, manipulation, and interpretation. Ann NY Acad Sci 1046:168–180PubMedCrossRefGoogle Scholar
  28. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav R 29:329–352CrossRefGoogle Scholar
  29. Hall PF (1969) Hormonal control of melanin synthesis in birds. Gen Comp Endocr 2:451–458CrossRefGoogle Scholar
  30. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218:384–387PubMedCrossRefGoogle Scholar
  31. Hasselquist D, Nilsson JA (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos T Roy Soc B 364:51–60CrossRefGoogle Scholar
  32. Ilmonen P, Hasselquist D, Langefors A, Wiehn J (2003) Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136:148–154PubMedCrossRefGoogle Scholar
  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 Columba livia. J Avian Biol 42:11–15CrossRefGoogle Scholar
  34. Jenni L, Winkler R (1994) Moult and ageing of European passerines. Academic, LondonGoogle Scholar
  35. Ketterson ED, Nolan V, Wolf L, Ziegenfus C (1992) Testosterone and avian life histories—effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). Am Nat 140:980–999CrossRefGoogle Scholar
  36. Laaksonen T, Adamczyk F, Ahola M, Möstl E, Lessells CM (2011) Yolk hormones and sexual conflict over parental investment in the pied flycatcher. Behav Ecol Sociobiol 65:257–264PubMedCrossRefGoogle Scholar
  37. Lehikoinen E (2001) Varpuslintujen sulkasadon tutkimus. Moult of Finnish passerines—an overview. Linnut-vuosikirja 2000. BirdLife Suomi, Helsinki, pp 55–65Google Scholar
  38. Lehtonen PK, Primmer CR, Laaksonen T (2009) Different traits affect gain of extrapair paternity and loss of paternity in the pied flycatcher, Ficedula hypoleuca. Anim Behav 77:1103–1110CrossRefGoogle Scholar
  39. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities—a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  40. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (2006) SAS system for mixed models. SAS Institute Inc., CaryGoogle Scholar
  41. Lundberg A, Alatalo R (1992) The pied flycatcher. Poyser, LondonGoogle Scholar
  42. Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299CrossRefGoogle Scholar
  43. McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247PubMedCrossRefGoogle Scholar
  44. McNab BK (1997) On the utility of uniformity in the definition of basal rate of metabolism. Physiol Zool 70:718–720PubMedGoogle Scholar
  45. Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996CrossRefGoogle Scholar
  46. 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 16:383–388CrossRefGoogle Scholar
  47. Moreno J, Morales J, Lobato E, Merino S, Tomas G, Martinez-de la Puente J (2005) Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca. Behav Ecol 16:931–937CrossRefGoogle Scholar
  48. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New YorkGoogle Scholar
  49. Müller W, Eens M (2009) Elevated yolk androgen levels and the expression of multiple sexually selected male characters. Horm Behav 55:175–181PubMedCrossRefGoogle Scholar
  50. Müller W, Deptuch K, Lopez-Rull I, Gil D (2007) Elevated yolk androgen levels benefit offspring development in a between-clutch context. Behav Ecol 18:929–936CrossRefGoogle Scholar
  51. Müller W, Vergauwen J, Eens M (2008) Yolk testosterone, postnatal growth and song in male canaries. Horm Behav 54:125–133PubMedCrossRefGoogle Scholar
  52. Müller W, Vergauwen J, Eens M (2009) Long-lasting consequences of elevated yolk testosterone levels on female reproduction. Behav Ecol Sociobiol 63:809–816CrossRefGoogle Scholar
  53. Navara KJ, Mendonça MT (2008) Yolk androgens as pleiotropic mediators of physiological processes: a mechanistic review. Comp Biochem Physiol A 150:378–386CrossRefGoogle Scholar
  54. Navara KJ, Hill GE, Mendonça MT (2006) Yolk androgen deposition as a compensatory strategy. Behav Ecol Sociobiol 60:392–398CrossRefGoogle Scholar
  55. Nilsson JÅ, Råberg L (2001) The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128:187–192CrossRefGoogle Scholar
  56. Nilsson JÅ, Granbom M, Råberg L (2007) Does the strength of an immune response reflect its energetic cost? J Avian Biol 38:488–494Google Scholar
  57. Nilsson JF, Tobler M, Nilsson JÅ, Sandell MI (2011) Long-lasting consequences of elevated yolk testosterone for metabolism in the zebra finch. Physiol Biochem Zool 84:287–291PubMedCrossRefGoogle Scholar
  58. Ojanen M, Orell M (1982) Onset of moult among breeding pied flycatchers (Ficedula hypoleuca) in Northern Finland. Vogelwarte 31:445–451Google Scholar
  59. Partecke J, Schwabl H (2008) Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Devel Neurobiol 68:1538–1548CrossRefGoogle Scholar
  60. Perez-Campo R, Lopez-Torres M, Cadenas S, Rojas C, Barja G (1998) The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol B 168:149–158PubMedCrossRefGoogle Scholar
  61. 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 40:225–230CrossRefGoogle Scholar
  62. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239CrossRefGoogle Scholar
  63. Rubolini D, Romano M, Martinelli R, Leoni B, Saino N (2006) Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav Ecol Sociobiol 59:549–560CrossRefGoogle Scholar
  64. 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 274:137–142Google Scholar
  65. Rutkowska J, Wilk T, Cichoń M (2007) Androgen-dependent maternal effects on offspring fitness in zebra finches. Behav Ecol Sociobiol 61:1211–1217CrossRefGoogle Scholar
  66. Ruuskanen S (2010) Maternal effects in birds—the ecological and evolutionary significance of yolk androgens and other egg components. Painosalama Oy, TurkuGoogle Scholar
  67. Ruuskanen S, Laaksonen T (2010) Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca). Horm Behav 57:119–127PubMedCrossRefGoogle Scholar
  68. 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 55:514–519PubMedCrossRefGoogle Scholar
  69. Ruuskanen S, Doligez B, Gustafsson L, Laaksonen T (2012a) Long-term effects of yolk androgens on phenotype and parental feeding behavior in a wild passerine. Behav Ecol Sociobiol 66:1201–1211CrossRefGoogle Scholar
  70. Ruuskanen S, Doligez B, Pitala N, Gustafsson L, Laaksonen T (2012b) Long-term fitness consequences of high yolk androgen levels: sons pay the costs. Funct Ecol 26:884–894CrossRefGoogle Scholar
  71. Salewski V, Altwegg R, Erni B, Falk KH, Bairlein F, Leisler B (2004) Moult of three Palaearctic migrants in their West African winter quarters. J Ornithol 145:109–116CrossRefGoogle Scholar
  72. Siitari H, Honkavaara J, Huhta E, Viitala J (2002) Ultraviolet reflection and female mate choice in the pied flycatcher, Ficedula hypoleuca. Anim Behav 63:97–102CrossRefGoogle Scholar
  73. Sirkiä PM, Laaksonen T (2009) Distinguishing between male and territory quality: females choose multiple traits in the pied flycatcher. Anim Behav 78:1051–1060CrossRefGoogle Scholar
  74. Sirkiä PM, Virolainen M, Laaksonen T (2010) Melanin coloration has temperature-dependent effects on breeding performance that may maintain phenotypic variation in a passerine bird. J Evol Biol 23:2385–2396PubMedCrossRefGoogle Scholar
  75. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572CrossRefGoogle Scholar
  76. Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56:491–497CrossRefGoogle Scholar
  77. Svensson E, Råberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912–919CrossRefGoogle Scholar
  78. Tobler M, Nilsson JA, Nilsson JF (2007) Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol Lett 3:408–410PubMedCrossRefGoogle Scholar
  79. Tobler M, Hasselquist D, Smith HG, Sandell MI (2010) Short- and long-term consequences of prenatal testosterone for immune function: an experimental study in the zebra finch. Behav Ecol Sociobiol 64:717–727CrossRefGoogle Scholar
  80. Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H (2005) Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol 74:675–682CrossRefGoogle Scholar
  81. Tschirren B, Fitze PS, Richner H (2007) Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? Am Nat 169:87–93PubMedCrossRefGoogle Scholar
  82. Uller T, Olsson M (2003) Prenatal exposure to testosterone increases ectoparasite susceptibility in the common lizard (Lacerta vivipara). Proc R Soc Lond B 270:1867–1870CrossRefGoogle Scholar
  83. Uller T, Astheimer L, Olsson M (2007) Consequences of maternal yolk testosterone for offspring development and survival: experimental test in a lizard. Funct Ecol 21:544–551CrossRefGoogle Scholar
  84. Vezina F, Wingfield TD (2005) The metabolic cost of egg production is repeatable. J Exp Biol 208:2533–2538PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Suvi Ruuskanen
    • 1
    • 2
  • Esa Lehikoinen
    • 1
  • Mikko Nikinmaa
    • 3
  • Heli Siitari
    • 4
  • Wolfgang Waser
    • 3
  • Toni Laaksonen
    • 1
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  2. 2.Department of Animal EcologyNetherlands Institute of Ecology (NIOO-KNAW)WageningenNetherlands
  3. 3.Division of Genetics and Physiology, Department of BiologyUniversity of TurkuTurkuFinland
  4. 4.Department of Biological and Environmental SciencesUniversity of JyväskyläJyväskyläFinland

Personalised recommendations