, Volume 34, Issue 1, pp 87–94 | Cite as

Embryonic exposure to maternal testosterone influences age-specific mortality patterns in a captive passerine bird

  • Hubert Schwabl
  • Donna HolmesEmail author
  • Rosemary Strasser
  • Alex Scheuerlein


Hormones are potent mediators of developmental programming and maternal epigenetic effects. In vertebrates, developmental exposure to maternal androgen hormones has been shown to impact multiple behavioral and physiological traits of progeny, but the possible consequences of this early exposure in terms of aging-related changes in mortality and fitness remain largely unexplored. Avian eggs naturally contain variable doses of maternal hormones—in particular, androgens—which have documented effects on embryo growth and differentiation as well as adult behavior and physiology. Here, we report that injections of a physiological dose of testosterone (T) into yolks of freshly laid eggs of a small, seasonally breeding songbird, the house sparrow (Passer domesticus), increased survivorship in a semi-natural aviary environment. In addition, survival effects of developmental T exposure were sex-dependent, with males generally having a higher risk of death. Separate analyses for young birds in their first year of life (from hatching up to the first reproductive period the following calendar year) and in adulthood (after the first breeding season) showed similar effects. For first-year birds, mortality risk was higher during the winter than during the period after fledging; for adults, mortality risk was higher during the reproductive than the non-reproductive phase (post-breeding molt and winter). T treatment did not affect nestling body mass, but resulted in higher body mass at 3–4 months of age; T and body mass at this age interacted to influence mortality risk. Embryonic exposure to maternal testosterone may result in lower adult mortality by modifying intrinsic physiological processes involved in health or aging over the lifespan of adult birds.


Developmental plasticity Maternal effect Non-genomic inheritance Aging Prenatal programming Mortality Yolk testosterone 



We thank M. Webster, R.E. Ricklefs, and two anonymous reviewers for comments on previous versions of the manuscript. B. Duskin, M. Leland, and C. Clark helped with raising the sparrows. Research was supported by grants of the Harry Frank Guggenheim Foundation (to H.S.) and of the National Institutes of Mental Health (no. MH4987 to H.S and no. HD F32HD08542 to R.S.).

Supplementary material

11357_2011_9222_MOESM1_ESM.doc (74 kb)
ESM 1 (DOC 74 kb)


  1. Arnold AP (2002) Concepts of genetic and hormonal induction of vertebrate sexual differentiation in the twentieth century, with special reference to the brain. In: Pfaff DW, Arnold AOP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior, vol iv. Academic, New York, pp 105–135CrossRefGoogle Scholar
  2. Badyaev AV, Hill GE, Beck ML, Dervan AA, Duckworth RA, McGraw KJ, Nolan PM, Whittingham LA (2002) Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295:316–318PubMedCrossRefGoogle Scholar
  3. Birkhead T, Schwabl H, Burke T (2001) Testosterone and maternal effects—integrating mechanisms and functions. Trends Ecol Evol 15:86–87CrossRefGoogle Scholar
  4. Bribiescas R, Ellison P (2008) How hormones mediate trade-offs in human health and disease. In: Stearns SC (ed) Evolution in health and disease. Oxford University Press, New York, pp 77–94Google Scholar
  5. Brown-Borg HM, Borg KE, Meliska CJ, Bartke A (1996) Dwarf mice and the ageing process. Nature 384:33PubMedCrossRefGoogle Scholar
  6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  7. Carey J, Judge D (2000) Longevity records: life spans of mammals, birds, amphibians, reptiles, and fish. Odense University Press, OdenseGoogle Scholar
  8. Collett D (2003) Modelling survival data in medical research. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  9. 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 Endocrinol 156:418–425PubMedCrossRefGoogle Scholar
  10. Daan S, Tinbergen JM (1997) Adaptation of life histories. In: Krebs JR, Davies NB (eds) Behavioral ecology: an evolutionary approach, 4th edn. Wiley, New York, pp 311–333Google Scholar
  11. Doblhammer G, Vaupel JW (2001) Lifespan depends on month of birth. Proc Natl Acad Sci U S A 98:2934–2939PubMedCrossRefGoogle Scholar
  12. Eising CM, Groothuis TTG (2002) Long-term effects of maternal yolk androgens: an experimental approach. Intern Soc Behavioral Ecology 9th Congr, Abstracts. pp 35–36Google Scholar
  13. Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull eggs: consequences for chick development. Proc R Soc Lond B 268:839–846CrossRefGoogle Scholar
  14. Finch CE (2007) The biology of human longevity: inflammation, nutrition, and aging in the evolution of lifespans. Elsevier, Amsterdam, p 626Google Scholar
  15. Finch CE, Rose MR (1995) Hormones and the physiological architecture of life history evolution. Q Rev Biol 70:1–52PubMedCrossRefGoogle Scholar
  16. Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  17. Fox CW, Mousseau TA (1998) Maternal effects as adaptations for transgenerational phenotypic plasticity in insects. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, OxfordGoogle Scholar
  18. Gebhardt-Henrich S, Richner H (1998) Causes of growth variation and its consequences for fitness. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Oxford University Press, New York, pp 324–340Google Scholar
  19. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  20. Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305:1733–1736PubMedCrossRefGoogle Scholar
  21. Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Phil Trans R Soc B 363:1647–1661PubMedCrossRefGoogle Scholar
  22. Groothuis TGG, Eising CM, Dijkstra C, Müller W (2005) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett 1:78–81PubMedCrossRefGoogle Scholar
  23. Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20PubMedCrossRefGoogle Scholar
  24. Harper JM, Galecki AT, Burke DT, Miller RA (2004) Body weight, hormones and T cell subsets as predictors of life span in genetically heterogeneous mice. Mech Ageing Dev 125:381–390PubMedCrossRefGoogle Scholar
  25. Hegner RE, Wingfield JC (1986) Gonadal development during autumn and winter in house sparrows. Condor 88(269–2):78Google Scholar
  26. Holmes DJ, Austad SN (1995) Birds as animal models for the comparative biology of aging: a prospectus. J Gerontol Biol Sci 50A:59–66CrossRefGoogle Scholar
  27. Holmes DJ, Martin K (2009) Special reviews in ornithology. A bird’s-eye view of aging: what’s in it for ornithologists? The Auk 126(1):1–23CrossRefGoogle Scholar
  28. Kirkwood TBL, Austad SN (2000) Why do we age? Nature 408:233–238PubMedCrossRefGoogle Scholar
  29. Klimkiewicz MK, Futcher AG (1987) Longevity records of North American birds: Coerbinae through Estrildidae. J Field Ornithol 58:318–333Google Scholar
  30. Lummaa V, Clutton-Brock T (2002) Early development, survival and reproduction in humans. Trends Ecol Evol 17:141–147CrossRefGoogle Scholar
  31. Martin TM, Schwabl H (2008) Variation in maternal effects and embryonic development among passerine bird species. Phil Trans R Soc B 363:1635–1645CrossRefGoogle Scholar
  32. Monaghan P (2008) Early development, phenotypic development and environmental change. Phil Trans R Soc B 363:1635–1645PubMedCrossRefGoogle Scholar
  33. Müller W, Lessells C, Kortsen P, von Engelhardt N (2007) Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. Am Nat 169:E84–E94PubMedCrossRefGoogle Scholar
  34. Müller W, Vergauwen J, Eens M (2009) Long-lasting consequences of elevated testosterone levels on female reproduction. Behav Ecol Sociobiol 63:809–816CrossRefGoogle Scholar
  35. Navara KJ, Mendonca MT (2006) Yolk testosterone stimulates growth and immunity in house finches. Physiol Biochem Zool 79:550–555PubMedCrossRefGoogle Scholar
  36. Partecke J, Schwabl H (2008) Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev Neurobiol 68:1538–1548PubMedCrossRefGoogle Scholar
  37. Perrins CM (1965) Population fluctuations and clutch size in the great tit Parus major. J Anim Ecol 34:601–647CrossRefGoogle Scholar
  38. Poopatanapong A (2002) Relationship between male badge size and female reproductive investment and mate choice in House Sparrow. MS thesis, Washington State University, Pullman, WashingtonGoogle Scholar
  39. Ricklefs R (2008) The evolution of senescence from a comparative perspective. Funct Ecol 22:379–392CrossRefGoogle Scholar
  40. Ringsby TH, Saether B-E, Solberg EJ (1998) Factors affecting juvenile survival in House Sparrow. Passer domesticus. J Avian Biol 29:241–247CrossRefGoogle Scholar
  41. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci U S A 90:11446–11450PubMedCrossRefGoogle Scholar
  42. Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol 114A:271–276CrossRefGoogle Scholar
  43. Schwabl H (1997) The contents of maternal testosterone in House Sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 84:406–408PubMedCrossRefGoogle Scholar
  44. Schwabl H (1998) Maternal hormonal effects on postnatal development. In: Adams NJ, Slotow RH (eds) Proc. 22. Intl. Ornithol. Congr. Durban, South Africa, CD-ROMGoogle Scholar
  45. Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386:231CrossRefGoogle Scholar
  46. Schwabl HM, Palacios G, Martin TE (2007) Selection for rapid embryo development correlates with embryo exposure to maternal androgens among passerine birds. Am Nat 170:196–206PubMedCrossRefGoogle Scholar
  47. Seckl JC (2001) Glucocorticoids, feto-placental 11β-hydroxysteroid dehydrogenase type 2 and early life origins of adult disease. Steroids 62:89–94CrossRefGoogle Scholar
  48. Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267:1451–1456CrossRefGoogle Scholar
  49. Sockman KW, Sharp PJ, Schwabl H (2006) Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behavior, and yolk androgen deposition. Biol Rev 81:629–666PubMedCrossRefGoogle Scholar
  50. Sonntag WE, Carter CS, Ikeno Y, Ekenstedt K, Carlson CS et al (2005) Adult-onset growth hormone and insulin-like growth factor I deficiency reduces neoplastic disease, modifies age-related pathology, and increases life span. Endocrinology 146:2920–2932PubMedCrossRefGoogle Scholar
  51. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  52. Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Horm Behav 47:503–512Google Scholar
  53. Sugiura N (1978) Further analysis of the data by Akaike’s information criterion and the finite corrections. Commun Stat, Theory Methods A7:13–26Google Scholar
  54. Summers-Smith JD (1998) The sparrows: a study of the genus Passer. A.D. Poyser Ltd, CaltonGoogle Scholar
  55. Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin-like signals. Science 299:1346–1351PubMedCrossRefGoogle Scholar
  56. Tobler M, Sandell MI (2007) Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata. Horm Behav 52:640–645PubMedCrossRefGoogle Scholar
  57. Tobler M, Sandell MI (2009) Sex-specific effects of prenatal testosterone on nestling plasma antioxidant capacity in the zebra finch. J Exp Biol 212:89–94PubMedCrossRefGoogle Scholar
  58. Tobler M, Nilsson J-Å, Nilsson JF (2007) Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol Lett 3:408–410PubMedCrossRefGoogle Scholar
  59. Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H (2005) Maternal yolk testosterone does not modulate parasite susceptibility in great tit nestlings. J Anim Ecol 74:675–682CrossRefGoogle Scholar
  60. Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23:432–438PubMedCrossRefGoogle Scholar
  61. 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 B 271:65–70CrossRefGoogle Scholar

Copyright information

© American Aging Association 2011

Authors and Affiliations

  • Hubert Schwabl
    • 1
  • Donna Holmes
    • 1
    Email author
  • Rosemary Strasser
    • 2
  • Alex Scheuerlein
    • 3
  1. 1.Center for Reproductive Biology and School of Biological SciencesWashington State UniversityPullmanUSA
  2. 2.Psychology DepartmentUniversity of Nebraska at OmahaOmahaUSA
  3. 3.Max Planck Institute for Demographic ResearchRostockGermany

Personalised recommendations