Investigating maternal hormones in avian eggs: Measurement, manipulation, and interpretation

Annals of the New York Academy of Sciences

Volumn 1046, Issue , 2005, Pages 168-180

  Groothuis, Ton G G ^a   Von Engelhardt, Nikolaus ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Androgens; Birds; Development; Egg quality, nongenomic inheritance; Maternal effects; Maternal hormones; Steroids

Indexed keywords

HORMONE; STEROID HORMONE;

CLUTCH SIZE; CONFERENCE PAPER; EGG; EGG LAYING; EMBRYO MORTALITY; ENVIRONMENTAL FACTOR; FOWL; HORMONE DETERMINATION; NONHUMAN;

AVES;

EID: 23744494714     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1196/annals.1343.014     Document Type: Conference Paper

References (51)

1. SCHWABL, H. 1993. Yolk is source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. USA 90: 11446-11450.
2. GROOTHUIS, T.G.G. et al. 2005. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29: 329-352.
3. COOKE, B., C.D. HEGSTROM, L.S. VILLENEUVE & S.M. BREEDLOVE. 1998. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front. Neuroendocrinol. 19: 323-362.
4. ROS, A.F., S.J. DIELEMAN & T.G. GROOTHUIS. 2002. Social stimuli, testosterone, and aggression in gull chicks: support for the challenge hypothesis. Horm. Behav. 41: 334-342.
5. RHEN, T. & D. CREWS. 2002. Variation in reproductive behaviour within a sex: neural systems and endocrine activation. J. Neuroendocrinol. 14: 517-531.
6. GROOTHUIS, T.G. & C. CARERE. 2005. Avian personalities: characterization and epigenesis. Neurosci. Biobehav. Rev. 29: 137-150.
7. WINGFIELD, J.C. et al. 1990. The challenge hypothesis-theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136: 829-846.
8. WEINSTOCK, M. 1997. Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci. Biobehav. Rev. 21: 1-10.
9. MCCORMICK, M.I. 1999. Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 118: 412-422.
10. LOVERN, M.B. & J. WADE. 2001. Maternal plasma and egg yolk testosterone concentrations during embryonic development in green anoles (Anolis carolinensis). Gen. Comp. Endocrinol. 124: 226-235.
11. BOWDEN, R.M., M.A. EWERT & C.E. NELSON. 2000. Environmental sex determination in a reptile varies seasonally and with yolk hormones. Proc. R. Soc. Lond. B Biol. Sci. 267: 1745-1749.
12. GLICKMAN, S.E. et al. 1987. Androstenedione may organize or activate sex-reversed traits in female spotted hyenas. Proc. Natl. Acad. Sci. USA. 84: 3444-3447.
13. HINES, M. et al. 2002. Testosterone during pregnancy and gender role behavior of pre-school children: a longitudinal, population study. Child Dev. 73: 1678-1687.
14. VON ENGELHARDT, N. & T.G. GROOTHUIS. 2005. Measuring steroid hormones in avian eggs. Ann. N.Y. Acad. Sci. 1046: 181-192.
15. EISING, C.M. 2003. Mother knows best? Costs and benefits of differential maternal hormone allocation in birds. Ph.D. thesis. University of Groningen. Groningen, the Netherlands.
16. HACKL, R. et al. 2003. Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). J. Comp. Physiol. [B] 173: 327-331.
17. LIPAR, J.L., E.D. KETTERSON, V. NOLAN, JR. & M. CASTO. 1999. Egg Yolk layers vary in the concentration of steroid hormones in two avian species. Gen. Comp. Endocrinol. 115: 220-227.
18. NAVARA, K.J., G.E. HILL & M.T. MENDONCA. 2005. Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol. Biochem. Zool. In press.
19. ELF, P.K. & A.J. FIVIZZANI. 2002. Changes in sex steroid levels in yolks of the leghorn chicken, Callus domesticus, during embryonic development. J. Exp. Zool. 293: 594-600.
20. EISING, C.M., W. MÜLLER, C. DIJKSTRA & T.G. GROOTHUIS. 2003. Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen. Comp. Endocrinol. 132: 241-247.
21. BRUGGEMAN, V., P. VAN AS & E. DECUYPERE. 2002. Developmental endocrinology of the reproductive axis in the chicken embryo. Comp. Biochem. Physiol. A 131: 839-846.
22. BALTHAZART, J. & E. ADKINS-REGAN. 2002. Sexual differentiation of brain and behavior in birds. In Hormones, Brain and Behaviour. D. Pfaff et al., Eds.: 223-301. Academic Press. San Diego.
23. HAYWARD, L.S. & J.C. WINGFIELD. 2004. Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen. Comp. Endocrinol. 135: 365-371.
24. CARERE, C. 2003. Personalities as epigenetic suites of traits. A study on a passerine bird. Ph.D. thesis. University of Groningen. Groningen, the Netherlands.
25. PETRIE, M., H. SCHWABL, N. BRANDE-LAVRIDSEN & T. BURKE. 2001. Sex differences in avian yolk hormone levels. Nature 412: 498-499.
26. MÜLLER, W., C.M. EISING, C. DIJKSTRA & T.G. GROOTHUIS. 2002. Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Callus gallus domesticus). Proc. R. Soc. Lond. B. Biol. Sci. 269: 2249-2255.
27. RUTSTEIN, A.N. et al. 2005. Sex-specific patterns of yolk androgen allocation depend upon maternal diet in the zebra finch. Behav. Ecol. 16: 62-69.
28. MÜLLER, W. 2004. Maternal phenotypic engineering: adaptation and constraint in prenatal maternal effects. Ph.D. thesis. University of Groningen. Groningen, the Netherlands.
29. EWEN, J.G., P. CASSEY & A.P. MØLLER. 2004. Facultative primary sex ratio variation: a lack of evidence in birds? Proc. R. Soc. Loud. B Biol. Sci. 271: 1277-1282.
30. GROOTHUIS, T.G. & H. SCHWABL. 2002. Determinants of within- and among-clutch variation in levels of maternal hormones in Black-Headed Gull eggs. Funct. Ecol. 16: 281-289.
31. ROYLE, N.J., P.F. SURAI & I.R. HARTLEY. 2001. Maternally derived androgcns and anti-oxidants in bird eggs: complementary but opposing effects? Behav. Ecol. 12: 381-385.
32. PILZ, K.M. et al. 2003. Interfeinale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Anim. Behav. 65: 841-850.
33. PERRIN, F.M.R., S. STAGEY, A.M.C. BURGESS & U. MITTWOCH. 1995. A quantitative investigation of gonadal feminization by diethylstilbestrol of genetically male embryos of the quail coturnix-coturnix-japonica. J. Reprod. Fertil. 103: 223-226.
34. LAY, D.C. & M.E. WILSON. 2002. Development of the chicken as a model for prenatal stress. J. Anim. Sci. 80: 1954-1961.
35. LIPAR, J.L. & E.D. KETTERSON. 2000. Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc. R. Soc. Lond. B Biol. Sci. 267: 2005-2010.
36. MÜLLER, W. et al. 2005. An experimental study on the causes of sex-biased mortality in the black-headed gull-the possible role of testosterone. J. Anim. Ecol. In press.
37. VON ENGELHARDT, N. 2004. Proximate control of avian sex allocation. A study on zebra finches. Ph.D. thesis. University of Groningen. Groningen, the Netherlands.
38. SOCKMAN, K.W. & H. SCHWABL. 2000. Yolk androgens reduce offspring survival. Proc. R. Soc. Lond. B Biol. Sci. 267: 1451-1456.
39. DIJKSTRA, C., S. DAAN & J.B. BUKER. 1990. Adaptive seasonal variation in the sex ratio of kestrel broods. Funct. Ecol. 4: 143-147.
40. GROOTHUIS, T.G., C.M. EISING, C. DIJKSTRA & W. MÜLLER. 2005. Balancing between costs and benefits of maternal hormone deposition in avian eggs. Proc. R. Soc. Lond. B Biol. Lett. 1:78-81.
41. SAINO, N. et al. 2003. Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc. R. Soc. Lond. B Biol. Sci. 270: 2485-2489.
42. EISING, C.M., C. EIKENAAR, H. SCHWABL & T.G. GROOTHUIS. 2001. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc. R. Soc. Lond. B Biol. Sci. 268: 839-846.
43. GIL, D., J. GRAVES, N. HAZON & A. WELLS. 1999. Male attractiveness and differential testosterone investment in zebra fineh eggs. Science 286: 126-128.
44. STRASSER, R. & H. SCHWABL. 2004. Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav. Ecol. Sociobiol. 56:491-497.
45. ELLIS, L.A., D.W. BORST & C.F. THOMPSON. 2001. Hatching asynchrony and maternal androgens in egg yolks of house wrens. J. Avian Biol. 32: 26-30.
46. MÜLLER, W. et al. 2004. Within-clutch patterns of yolk testosterone vary with the onset of incubation in black-headed gulls. Behav. Ecol. 15: 893-897.
47. GOULD, S.J. & E.S. VRBA. 1982. Exaptation-a missing term in the science of form. Paleobiology 8: 4-15.
48. SCHWABL, H. 1996. Environment modifies the testosterone levels of a female bird and its eggs. J. Exp. Zool. 276: 157-163.
49. TANVEZ, A. et al. 2004. Sexually attractive phrases increase yolk androgen deposition in Canaries (Serinus canaria). Gen. Comp. Endocrinol. 138: 113-120.
50. VERBOVEN, N., P. MONAGHAN, D.M. EVANS, et al. 2003. Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc. R. Soc. Lond. B Biol. Sci. 270: 2223-2232.
51. BAHR, J.M., S.C. WANG, M.Y. HUANG & F.O. CALVO. 1983. Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biol. Reprod. 29: 326-334.