Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Nov 7;270(1530):2223–2232. doi: 10.1098/rspb.2003.2496

Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus).

Nanette Verboven 1, Pat Monaghan 1, Darren M Evans 1, Hubert Schwabl 1, Neil Evans 1, Christine Whitelaw 1, Ruedi G Nager 1
PMCID: PMC1691499  PMID: 14613608

Abstract

It has been proposed that the maternal androgens in avian egg yolk enhance offspring fitness by accelerating growth and improving competitive ability. Because egg quality is strongly influenced by maternal condition, we predicted that females in good condition would produce high-quality eggs with relatively high androgen content. We experimentally enhanced maternal condition by supplementary feeding lesser black-backed gulls (Larus fuscus) during egg formation and compared the concentrations of androstenedione (A4), 5alpha-dihydrotestosterone (DHT) and testosterone (T) in their eggs with those in eggs laid by control females. We also measured circulating levels of T in females immediately after laying. Egg androgens could affect offspring performance directly through chick development and/or indirectly through changes in the competitive ability of a chick relative to its siblings. To avoid confounding these two routes, and to separate effects operating through the egg itself with those operating through experimental changes in parental chick rearing capacity, we fostered eggs from both maternal treatment groups singly into the nests of unmanipulated parents. Contrary to expectation, mothers with experimentally enhanced body condition laid eggs with lower levels of androgens, while exhibiting higher circulating T concentrations post-laying. Despite these lower levels of egg androgen, offspring hatched from eggs laid by mothers in good condition did not show reduced growth or survival when reared in the absence of sibling competition. Our results demonstrate that yolk androgen concentrations vary with the body condition of the female at the time of egg formation and that females in good condition reduced the yolk androgen content of their eggs without altering offspring performance.

Full Text

The Full Text of this article is available as a PDF (230.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arcos M. Steroids in egg yolk. Steroids. 1972 Jan;19(1):25–34. doi: 10.1016/0039-128x(72)90024-4. [DOI] [PubMed] [Google Scholar]
  2. Bahr J. M., Wang S. C., Huang M. Y., Calvo F. O. Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biol Reprod. 1983 Sep;29(2):326–334. doi: 10.1095/biolreprod29.2.326. [DOI] [PubMed] [Google Scholar]
  3. Blount Jonathan D., Surai Peter F., Nager Ruedi G., Houston David C., Møller Anders Pape, Trewby Michael L., Kennedy Malcolm W. Carotenoids and egg quality in the lesser blackbacked gull Larus fuscus: a supplemental feeding study of maternal effects. Proc Biol Sci. 2002 Jan 7;269(1486):29–36. doi: 10.1098/rspb.2001.1840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buchanan K. L., Evans M. R., Goldsmith A. R., Bryant D. M., Rowe L. V. Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc Biol Sci. 2001 Jul 7;268(1474):1337–1344. doi: 10.1098/rspb.2001.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Christians Julian K. Avian egg size: variation within species and inflexibility within individuals. Biol Rev Camb Philos Soc. 2002 Feb;77(1):1–26. doi: 10.1017/s1464793101005784. [DOI] [PubMed] [Google Scholar]
  6. Doi O., Takai T., Nakamura T., Tanabe Y. Changes in the pituitary and plasma LH, plasma and follicular progesterone and estradiol, and plasma testosterone and estrone concentrations during the ovulatory cycle of the quail (Coturnix coturnix japonica). Gen Comp Endocrinol. 1980 Jun;41(2):156–163. doi: 10.1016/0016-6480(80)90139-2. [DOI] [PubMed] [Google Scholar]
  7. Duckworth R. A., Mendonça M. T., Hill G. E. A condition dependent link between testosterone and disease resistance in the house finch. Proc Biol Sci. 2001 Dec 7;268(1484):2467–2472. doi: 10.1098/rspb.2001.1827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dufty A. M., Jr Testosterone and survival: a cost of aggressiveness? Horm Behav. 1989 Jun;23(2):185–193. doi: 10.1016/0018-506x(89)90059-7. [DOI] [PubMed] [Google Scholar]
  9. Eising C. M., Eikenaar C., Schwabl H., Groothuis T. G. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc Biol Sci. 2001 Apr 22;268(1469):839–846. doi: 10.1098/rspb.2001.1594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Elf Pamela K., Fivizzani Albert J. Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool. 2002 Nov 1;293(6):594–600. doi: 10.1002/jez.10169. [DOI] [PubMed] [Google Scholar]
  11. French J. B., Jr, Nisbet I. C., Schwabl H. Maternal steroids and contaminants in common tern eggs: a mechanism of endocrine disruption? Comp Biochem Physiol C Toxicol Pharmacol. 2001 Jan;128(1):91–98. doi: 10.1016/s1532-0456(00)00181-2. [DOI] [PubMed] [Google Scholar]
  12. Gil D., Graves J., Hazon N., Wells A. Male attractiveness and differential testosterone investment in zebra finch eggs. Science. 1999 Oct 1;286(5437):126–128. doi: 10.1126/science.286.5437.126. [DOI] [PubMed] [Google Scholar]
  13. Godsave Susan F., Lohmann Ragna, Vloet Rianka P. M., Gahr Manfred. Androgen receptors in the embryonic zebra finch hindbrain suggest a function for maternal androgens in perihatching survival. J Comp Neurol. 2002 Nov 4;453(1):57–70. doi: 10.1002/cne.10391. [DOI] [PubMed] [Google Scholar]
  14. Griffiths R., Double M. C., Orr K., Dawson R. J. A DNA test to sex most birds. Mol Ecol. 1998 Aug;7(8):1071–1075. doi: 10.1046/j.1365-294x.1998.00389.x. [DOI] [PubMed] [Google Scholar]
  15. Grossman C. J. Regulation of the immune system by sex steroids. Endocr Rev. 1984 Summer;5(3):435–455. doi: 10.1210/edrv-5-3-435. [DOI] [PubMed] [Google Scholar]
  16. Hammond R. W., Olson D. M., Frenkel R. B., Biellier H. V., Hertelendy F. Prostaglandins and steroid hormones in plasma and ovarian follicles during the ovulation cycle of the domestic hen (Gallus domesticus). Gen Comp Endocrinol. 1980 Oct;42(2):195–202. doi: 10.1016/0016-6480(80)90188-4. [DOI] [PubMed] [Google Scholar]
  17. Henry M. H., Burke W. H. The effects of in ovo administration of testosterone or an antiandrogen on growth of chick embryos and embryonic muscle characteristics. Poult Sci. 1999 Jul;78(7):1006–1013. doi: 10.1093/ps/78.7.1006. [DOI] [PubMed] [Google Scholar]
  18. Hews D. K., Knapp R., Moore M. C. Early exposure to androgens affects adult expression of alternative male types in tree lizards. Horm Behav. 1994 Mar;28(1):96–115. doi: 10.1006/hbeh.1994.1008. [DOI] [PubMed] [Google Scholar]
  19. Lipar J. L., Ketterson E. D. Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc Biol Sci. 2000 Oct 7;267(1456):2005–2010. doi: 10.1098/rspb.2000.1242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Metcalfe N. B., Monaghan P. Compensation for a bad start: grow now, pay later? Trends Ecol Evol. 2001 May 1;16(5):254–260. doi: 10.1016/s0169-5347(01)02124-3. [DOI] [PubMed] [Google Scholar]
  21. Müller Wendt, Eising Corine M., Dijkstra Cor, Groothuis Ton G. G. Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Gallus gallus domesticus). Proc Biol Sci. 2002 Nov 7;269(1506):2249–2255. doi: 10.1098/rspb.2002.2159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nager R. G., Monaghan P., Griffiths R., Houston D. C., Dawson R. Experimental demonstration that offspring sex ratio varies with maternal condition. Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):570–573. doi: 10.1073/pnas.96.2.570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ottinger M. A. Sexual differentiation of neuroendocrine systems and behavior. Poult Sci. 1989 Jul;68(7):979–989. doi: 10.3382/ps.0680979. [DOI] [PubMed] [Google Scholar]
  24. Peters A. Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc Biol Sci. 2000 May 7;267(1446):883–889. doi: 10.1098/rspb.2000.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Popescu O., Misevic G. N. Self-recognition by proteoglycans. Nature. 1997 Mar 20;386(6622):231–232. doi: 10.1038/386231b0. [DOI] [PubMed] [Google Scholar]
  26. Råberg L., Grahn M., Hasselquist D., Svensson E. On the adaptive significance of stress-induced immunosuppression. Proc Biol Sci. 1998 Sep 7;265(1406):1637–1641. doi: 10.1098/rspb.1998.0482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schwabl H. Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool. 1996 Oct 1;276(2):157–163. doi: 10.1002/(SICI)1097-010X(19961001)276:2<157::AID-JEZ9>3.0.CO;2-N. [DOI] [PubMed] [Google Scholar]
  28. Schwabl H. Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A Physiol. 1996 Jul;114(3):271–276. doi: 10.1016/0300-9629(96)00009-6. [DOI] [PubMed] [Google Scholar]
  29. Schwabl H. The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften. 1997 Sep;84(9):406–408. doi: 10.1007/s001140050418. [DOI] [PubMed] [Google Scholar]
  30. Sheffield J. W., O'Shaughnessy P. J. Effect of injection of gonadotrophin-releasing hormone on testicular steroidogenesis in the hypogonadal (hpg) mouse. J Reprod Fertil. 1989 Jul;86(2):609–617. doi: 10.1530/jrf.0.0860609. [DOI] [PubMed] [Google Scholar]
  31. Sockman K. W., Schwabl H. Yolk androgens reduce offspring survival. Proc Biol Sci. 2000 Jul 22;267(1451):1451–1456. doi: 10.1098/rspb.2000.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Williams T. D. Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev Camb Philos Soc. 1994 Feb;69(1):35–59. doi: 10.1111/j.1469-185x.1994.tb01485.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES