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

Proceedings of the Royal Society B: Biological Sciences

Volumn 270, Issue 1530, 2003, Pages 2223-2232

  Verboven, Nanette ^a   Monaghan, Pat ^a   Evans, Darren M ^a,d   Schwabl, Hubert ^b   Evans, Neil ^c   Whitelaw, Christine ^c   Nager, Ruedi G ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

Author keywords

Larus fuscus; Maternal condition; Offspring performance; Plasma testosterone; Supplemental feeding; Yolk androgens

Indexed keywords

ANDROGEN; ANDROSTANOLONE; ANDROSTENEDIONE; TESTOSTERONE;

BODY CONDITION; DEVELOPMENTAL BIOLOGY; EGG; FITNESS; FOOD SUPPLEMENTATION; MATERNAL EFFECT; SEABIRD;

ANIMAL BEHAVIOR; ANIMAL FOOD; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EGG LAYING; EGG YOLK; FEMALE; FOWL; GROWTH; MALE; MATERNAL CARE; NONHUMAN; PRIORITY JOURNAL; SIBLING; SURVIVAL; TESTOSTERONE BLOOD LEVEL; TISSUE LEVEL;

ANIMALIA; AVES; GALLIFORMES; LARUS; LARUS FUSCUS;

EID: 0242721423     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2003.2496     Document Type: Article

References (66)

1. Adkins-Regan, E., Ottinger, M. A. & Park, J. 1995 Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J. Exp. Zool. 271, 466-470.
2. Alonso-Alvarez, C. 2001 Effects of testosterone implants on pair behaviour during incubation in the yellow-legged gull Larus cachinnans. J. Avian Biol. 32, 326-332.
3. Alonso-Alvarez, C. & Velando, A. 2001 Effect of testosterone on the behaviour of yellow-legged gulls (Larus cachinnans) in a high-density colony during the courtship period. Ethol. Ecol. Evol. 13, 341-349.
4. Arcos, M. 1972 Steroids in egg yolk. Steroids 19, 25-34.
5. Bahr, J. M., Wang, S.-C., Huang, M. Y. & Calvo, F. O. 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.
6. Bernardo, J. 1996 Maternal effects in animal ecology. Am. Zool. 36, 83-105.
7. Blount, J. D., Surai, P. F., Nager, R. G., Houston, D. C., Møller, A. P., Trewby, M. L. & Kennedy, M. W. 2002 Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc. R. Soc. Lond. B 269, 29-36. (DOI 10.1098/rspb.2001. 1840.)
8. Bolton, M., Monaghan, P. & Houston, D. C. 1991 An improved technique for estimating pectoral muscle protein from body measurements in gulls. Ibis 133, 264-270.
9. Bolton, M., Houston, D. & Monaghan, P. 1992 Nutritional constraints on egg formation in the lesser black-backed gull: an experimental study. J. Anim. Ecol. 61, 521-532.
10. Bolton, M., Monaghan, P. & Houston, D. C. 1993 Proximate determination of clutch size in lesser black-backed gulls: the roles of food supply and body condition. Can. J. Zool. 71, 273-279.
11. Buchanan, K. L., Evans, M. R., Goldsmith, A. R., Bryant, D. M. & Rowe, L. V. 2001 Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc. R. Soc. Lond. B 268, 1337-1344. (DOI 10.1098/rspb.2001.1669.)
12. Christians, J. K. 2002 Avian egg size: variation within species and inflexibility within individuals. Biol. Rev. 77, 1-26.
13. Clark, M. M. & Galef Jr, B. G. 1995 Prenatal influences on reproductive life history strategies. Trends Ecol. Evol. 10, 151-153.
14. Doi, O., Takai, T., Nakamura, T. & Tanabe, Y. 1980 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. 41, 156-163.
15. Duckworth, R. A., Mendonça, M. T. & Hill, G. E. 2001 A condition dependent link between testosterone and disease resistance in the house finch. Proc. R. Soc. Lond. B 268, 2467-2472. (DOI 10.1098/rspb.2001.1827.)
16. Dufty, A. M. 1989 Testosterone and survival: a cost of aggressiveness? Horm. Behav. 23, 185-193.
17. Eising, C. M., Eikenaar, C., Schwabl, H. & Groothuis, T. G. G. 2001 Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc. R. Soc. Lond. B 268, 839-846. (DOI 10.1098/rspb.2001.1594.)
18. Elf, P. K. & Fivizzani, A. J. 2002 Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J. Exp. Zool. 293, 594-600.
19. French Jr, J. B., Nisbet, I. C. T. & Schwabl, H. 2001 Maternal steroids and contaminants in common tern eggs: a mechanism of endocrine disruption? Comp. Biochem. Physiol. C 128, 91-98.
20. Gasparini, J., McCoy, K. D., Haussy, C., Tveraa, T. & Boulinier, T. 2001 Induced maternal response to the Lyme disease sprirochaete Borrelia burgdorferi sensu lato in a colonial sea-bird, the kittiwake Rissa tridactyla. Proc. R. Soc. Lond. B 268, 1-4. (DOI 10.1098/rspb.2000.1411.)
21. Gil, D., Graves, J., Hazon, N. & Wells, A. 1999 Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286, 126-128.
22. Godsave, S. F., Lohmann, R., Vloet, R. P. M. & Gahr, M. 2002 Androgen receptors in the embryonic zebra finch hindbrain suggest a function for maternal androgens in peri-hatching survival. J. Comp. Neurol. 453, 57-70.
23. Griffiths, R. 1992 Sex-biased mortality in the lesser black-backed gull Larus fuscus during the nestling stage. Ibis 134, 237-244.
24. Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. G. 1998 A DNA test to sex most birds. Mol. Ecol. 7, 1071-1075.
25. Groothuis, T. & Meeuwissen, G. 1992 The influence of testosterone on the development and fixation of the from of displays in two age classes of young black-headed gulls. Anim. Behav. 43, 189-208.
26. Groothuis, T. G. & Schwabl, H. 2002 Determinants of within-and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Funct. Ecol. 16, 281-289.
27. Grossman, C. J. 1984 Regulation of the immune system by sex steroids. Endocr. Rev. 5, 435-455.
28. Hammond, R. W., Olson, D. M., Frenkel, R. B., Biellier, H. V. & Hertelendy, F. 1980 Prostaglandins and steroid hormones in plasma and ovarian follicles during the ovulation cycle of the domestic hen (Gallus domesticus). Gen. Comp. Endrocrinol. 42, 195-202.
29. Henry, M. H. & Burke, W. H. 1999 The effects of in ovo administration of testosterone or an antiandrogen on growth of chick embryos and embryonic muscle characteristics. Poultry Sci. 78, 1006-1013.
30. Hews, D. K., Knapp, R. & Moore, M. C. 1994 Early exposure to androgens affects adult expression of alternative male types in tree lizards. Horm. Behav. 28, 96-115.
31. Ketterson, E. D., Nolan Jr, V., Wolf, L. & Ziegenfus, C. 1992 Testosterone and avian life histories: effects of experimentally elevated testosterone on behaviour and correlates of fitness in the dark-eyed junco (Junco hyemalis). Am. Nat. 140, 980-999.
32. Lipar, J. L. 2001 Yolk steroids and the development of the hatching muscle in nestling European starlings. J. Avian Biol. 32, 231-238.
33. Lipar, J. L. & Ketterson, E. D. 2000 Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc. R. Soc. Lond. B 267, 2005-2010. (DOI 10.1098/rspb.2000. 1242.)
34. Lipar, J. L., Ketterson, E. D. & Nolan Jr, V. 1999 Intraclutch variation in testosterone content of red-winged blackbird eggs. Auk 116, 231-235.
35. McCorkle, F., Olah Jr, I. & Glick, B. 1980 The morphology of the phytohemagglutinin-induced cell response in the chicken's wattle. Poultry Sci. 59, 616-623.
36. McCormick, M. I. 1998 Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79, 1873-1883.
37. Metcalfe, N. B. & Monaghan, P. 2001 Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16, 248-254.
38. Monaghan, P. & Nager, R. G. 1997 Why don't birds lay more eggs? Trends Ecol. Evol. 12, 270-274.
39. Mousseau, T. A. & Fox, C. W. 1998 The adaptive significance of maternal effects. Trends Ecol. Evol. 13, 403-407.
40. Müller, W., Eising, C. M., Dijkstra, C. & Groothuis, T. G. G. 2002 Sex differences in yolk hormones depend on maternal social status in leghorn chickens (Gallus gallus domesticus). Proc. R. Soc. Lond. B 269, 2249-2255. (DOI 10.1098/rspb. 2002.2159.)
41. Nager, R. G., Monaghan, P., Griffiths, R., Houston, D. C. & Dawson, R. 1999 Experimental demonstration that offspring sex ratio varies with maternal condition. Proc. Natl Acad. Sci. USA 96, 570-573.
42. Nager, R. G., Monaghan, P. & Houston, D. C. 2000 Within-clutch trade-offs between the number and quality of eggs: experimental manipulations in gulls. Ecology 81, 1339-1350.
43. Nolan Jr, V., Ketterson, E. D., Ziegenfus, C., Cullen, D. P. & Chandler, C. R. 1992 Testosterone and avian life histories: effects of experimentally elevated testosterone on prebasic molt and survival in male dark-eyed juncos. Condor 94, 364-370.
44. Ottinger, M. A. 1989 Sexual differentiation of neuroendocrine systems and behavior. Poultry Sci. 68, 979-989.
45. Peters, A. 2000 Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proc. R. Soc. Lond. B 267, 883-889. (DOI 10.1098/rspb.2000. 1085.)
46. Pilz, K. M., Smith, H. G., Sandell, M. I. & Schwabl, H. 2003 Interfemale variation in egg yolk androgen allocation in the European starling: do high quality females invest more? Anim. Behav. 65, 841-850.
47. Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. 1998 On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. B 265, 1637-1641. (DOI 10.1098/rspb.1998.0482.)
48. Ramos-Fernandez, G., Nunez de la Mora, A., Wingfield, J. C. & Drummond, H. 2000 Endocrine correlates of dominance in chicks of the blue-footed booby (Sula nebouxii): testing the challenge hypothesis. Ethol. Ecol. Evol. 12, 27-34.
49. Reed, W. L. & Vleck, C. M. 2001 Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128, 164-171.
50. Roitt, I., Brostoff, J. & Male, D. 1996 Immunology, 4th edn. London: Mosby.
51. Royle, N. J. & Hamer, K. C. 1998 Hatching asynchrony and sibling size hierarchies in gulls: effects on parental investment decisions, brood reduction and reproductive success. J. Avian Biol. 29, 266-272.
52. Royle, N. J., Surai, P. F., McCartney, R. J. & Speake, B. K. 1999 Parental investment and egg yolk lipid composition in gulls. Funct. Ecol. 13, 298-306.
53. Royle, N. J., Surai, P. F. & Hartley, I. R. 2001 Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav. Ecol. 12, 381-385.
54. SAS Institute 2001 SAS/STAT software, release 8.02. Cary, NC: SAS Institute, Inc.
55. Schwabl, H. 1993 Yolk is a source of maternal testosterone for developing birds. Proc. Natl Acad. Sci. USA 90, 11 446-11 450.
56. Schwabl, H. 1996a Maternal testosterone in the avian egg enhances postnatal growth. Comp. Biochem. Physiol. A 114, 271-276.
57. Schwabl, H. 1996b Environment modifies the testosterone levels of a female bird and its eggs. J. Exp. Zool. 276, 157-163.
58. Schwabl, H. 1997a Maternal steroid hormones in the egg. In Perspectives in avian endocrinology (ed. S. Harvey & R. J. Etches), pp. 3-13. Bristol: Journal of Endocrinology Limited.
59. Schwabl, H. 1997b The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 84, 406-408.
60. Schwabl, H., Mock, D. W. & Gieg, J. A. 1997 A hormonal mechanism for parental favouritism. Nature 386, 231.
61. Sheffield, J. W. & O'Shaughnessy, P. J. 1989 Effect of injection of gonadothrophin-releasing hormone on testicular steroidgenesis in the hypogonadal (hpg) mouse. J. Reprod. Fert. 86, 609-617.
62. Sockman, K. W. & Schwabl, H. 2000 Yolk androgens reduce offspring survival. Proc. R. Soc. Lond. B 267, 1451-1456. (DOI 10.1098/rspb.2000.1163.)
63. Whittingham, L. A. & Schwabl, H. 2002 Maternal testosterone in tree swallow eggs varies with female aggression. Anim. Behav. 63, 63-67.
64. Williams, J. D. 1994 Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol. Rev. 68, 35-69.
65. Wingfield, J. C., Newman, A. L., Hunt Jr, G. L. & Farner, D. S. 1982 Endocrine aspects of female-female pairing in the Western gull (Larus occidentalis wymani). Anim. Behav. 30, 9-22.
66. Winkler, D. W. 1993 Testosterone in egg yolks: an ornithologist's perspective. Proc. Natl Acad. Sci. USA 90, 11 439-11 441.