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

Age

Volumn 34, Issue 1, 2012, Pages 87-94

  Schwabl, Hubert ^a   Holmes, Donna ^a   Strasser, Rosemary ^b   Scheuerlein, Alex ^c  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

^c MAX PLANCK INSTITUTE FOR DEMOGRAPHIC RESEARCH   (Germany)

Author keywords

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

Indexed keywords

TESTOSTERONE; ANDROGEN;

ADULTHOOD; ARTICLE; BODY MASS; BREEDING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EGG LAYING; EGG YOLK; EMBRYO; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; FEMALE; HATCHING; HORMONE ACTION; LIFESPAN; MALE; MORTALITY; NESTLING; NONHUMAN; PROGENY; SEX DIFFERENCE; SONGBIRD; SURVIVAL TIME; AGING; ANIMAL; ANIMAL EMBRYO; DRUG EFFECT; MATERNAL BEHAVIOR; RISK ASSESSMENT; RISK FACTOR; SEASON; SEXUAL BEHAVIOR; SPARROW; SURVIVAL;

AGING; ANDROGENS; ANIMALS; EGG YOLK; EMBRYO, NONMAMMALIAN; MATERNAL BEHAVIOR; RISK ASSESSMENT; RISK FACTORS; SEASONS; SEXUAL BEHAVIOR, ANIMAL; SPARROWS; SURVIVAL ANALYSIS; TESTOSTERONE;

EID: 84862325214     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-011-9222-8     Document Type: Article

References (61)

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 105-135
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 295:316-318
3. Birkhead T, Schwabl H, Burke T (2001) Testosterone and maternal effects - integrating mechanisms and functions. Trends Ecol Evol 15:86-87
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 77-94
5. Brown-Borg HM, Borg KE, Meliska CJ, Bartke A (1996) Dwarf mice and the ageing process. Nature 384:33
6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
7. Carey J, Judge D (2000) Longevity records: life spans of mammals, birds, amphibians, reptiles, and fish. Odense University Press, Odense
8. Collett D (2003) Modelling survival data in medical research. Chapman & Hall/CRC, Boca Raton
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 156:418-425
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 311-333
11. Doblhammer G, Vaupel JW (2001) Lifespan depends on month of birth. Proc Natl Acad Sci U S A 98:2934-2939
12. Eising CM, Groothuis TTG (2002) Long-term effects of maternal yolk androgens: an experimental approach. Intern Soc Behavioral Ecology 9th Congr, Abstracts. pp 35-36
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 268:839-846
14. Finch CE (2007) The biology of human longevity: inflammation, nutrition, and aging in the evolution of lifespans. Elsevier, Amsterdam, p 626
15. Finch CE, Rose MR (1995) Hormones and the physiological architecture of life history evolution. Q Rev Biol 70:1-52
16. Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 139:603-622
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, Oxford
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 324-340
19. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126-128
20. Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305:1733-1736
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 363:1647-1661
22. Groothuis TGG, Eising CM, Dijkstra C, Müller W (2005) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett 1:78-81
23. Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5-20
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 125:381-390
25. Hegner RE, Wingfield JC (1986) Gonadal development during autumn and winter in house sparrows. Condor 88(269-2):78
26. Holmes DJ, Austad SN (1995) Birds as animal models for the comparative biology of aging: a prospectus. J Gerontol Biol Sci 50A:59-66
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):1-23
28. Kirkwood TBL, Austad SN (2000) Why do we age? Nature 408:233-238
29. Klimkiewicz MK, Futcher AG (1987) Longevity records of North American birds: Coerbinae through Estrildidae. J Field Ornithol 58:318-333
30. Lummaa V, Clutton-Brock T (2002) Early development, survival and reproduction in humans. Trends Ecol Evol 17:141-147
31. Martin TM, Schwabl H (2008) Variation in maternal effects and embryonic development among passerine bird species. Phil Trans R Soc B 363:1635-1645
32. Monaghan P (2008) Early development, phenotypic development and environmental change. Phil Trans R Soc B 363:1635-1645
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-E94
34. Müller W, Vergauwen J, Eens M (2009) Long-lasting consequences of elevated testosterone levels on female reproduction. Behav Ecol Sociobiol 63:809-816
35. Navara KJ, Mendonca MT (2006) Yolk testosterone stimulates growth and immunity in house finches. Physiol Biochem Zool 79:550-555
36. Partecke J, Schwabl H (2008) Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev Neurobiol 68:1538-1548
37. Perrins CM (1965) Population fluctuations and clutch size in the great tit Parus major. J Anim Ecol 34:601-647
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, Washington
39. Ricklefs R (2008) The evolution of senescence from a comparative perspective. Funct Ecol 22:379-392
40. Ringsby TH, Saether B-E, Solberg EJ (1998) Factors affecting juvenile survival in House Sparrow. Passer domesticus. J Avian Biol 29:241-247
41. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci U S A 90:11446-11450
42. Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol 114A:271-276
43. Schwabl H (1997) The contents of maternal testosterone in House Sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 84:406-408
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-ROM
45. Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386:231
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 170:196-206
47. Seckl JC (2001) Glucocorticoids, feto-placental 11β-hydroxysteroid dehydrogenase type 2 and early life origins of adult disease. Steroids 62:89-94
48. Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267:1451-1456
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 81:629-666
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 146:2920-2932
51. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
52. Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Horm Behav 47:503-512
53. Sugiura N (1978) Further analysis of the data by Akaike's information criterion and the finite corrections. Commun Stat, Theory Methods A7:13-26
54. Summers-Smith JD (1998) The sparrows: a study of the genus Passer. A.D. Poyser Ltd, Calton
55. Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin-like signals. Science 299:1346-1351
56. Tobler M, Sandell MI (2007) Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata. Horm Behav 52:640-645
57. Tobler M, Sandell MI (2009) Sex-specific effects of prenatal testosterone on nestling plasma antioxidant capacity in the zebra finch. J Exp Biol 212:89-94
58. Tobler M, Nilsson J-Å, Nilsson JF (2007) Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol Lett 3:408-410
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 74:675-682
60. Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23:432-438
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 271:65-70