Present address: J. D. Blount, Centre for Ecology and Conservation, University of Exeter in Cornwall, UK
Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment
Version of Record online: 30 JAN 2006
Journal of Evolutionary Biology
Volume 19, Issue 4, pages 1304–1313, July 2006
How to Cite
GROOTHUIS, T. G. G., EISING, C. M., BLOUNT, J. D., SURAI, P., APANIUS, V., DIJKSTRA, C. and MÜLLER, W. (2006), Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. Journal of Evolutionary Biology, 19: 1304–1313. doi: 10.1111/j.1420-9101.2005.01072.x
- Issue online: 16 FEB 2006
- Version of Record online: 30 JAN 2006
- Received 10 August 2005; revised 16 November 2005; accepted 21 November 2005
- 1998. Ontogeny of immune function. In: Avian Growth and Development – Evolution Within the Altricial–Precocial (J.M.Starck & R.E.Ricklefs, eds), pp. 203–222. Oxford University Press, Oxford.
- 1983. Serum-proteins of wild turkey vultures (Cathartes aura). Comp. Biochem. Physiol. B 76: 907–913. , &
- 1998. Effects of ageing and oestrogens on the localization of immunoglobulin-containing cells in the chicken ovary. J Reprod. Fertil. 114: 11–16. , &
- 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. , , , , , &
- 2003. Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300: 125–127. , , &
- 2004. Egg laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proc. R. Soc. Lond. B 3 (Suppl): 79–81. , , &
- 2003. Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc. R. Soc. Lond. B 271 (Suppl. 3): 110–113.
- 1994. Egg predation in the Herring Gull Larus argentatus: why does it vary so much between nests? Ardea 82: 223–230. &
- 1986. Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67: 1206–1218. &
- 1990. Metabolism of carotenoid pigments in birds. FASEB J. 4: 2969–2977.
- 2002. Parasite-induced maternal response in a natural bird population. J. Anim. Ecol. 71: 247–252. , , , &
- 2002. Avian egg size: variation within species and inflexibility within individuals. Biol. Rev. 77: 1–26.
- 2000. Sexual dimorphism in house sparrow eggs. Behav. Ecol. Sociobiol. 48: 353–357. , , &
- 2001. Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling. J. Evol. Biol. 14: 829–834. , , &
- Cramp, S. & Simmons, K.E.L. (eds) 1983. Handbook of the Birds of Europe, the Middle East and North Africa: the Birds of the Western Paleartic. Volume III: Waders to Gulls. Oxford University Press, Oxford.
- 1978. Metabolism and passive transfer of immunoglobulins in the turkey hen. Am. J. Vet. Res. 39: 1472–1481. , &
- 2000. Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav. Ecol. 11: 654–662. , , &
- 2003. Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim. Behav. 66: 1027–1034. &
- 2001. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc. R. Soc. Lond. B 268: 839–846. , , &
- 2003. Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen. Comp. Endocrinol. 132: 241–247. , , &
- 2002. Changes in sex steroid levels in yolks of the Leghorn chicken, Gallus domesticus, during embryonic development. J. Exp. Zool. 293: 594–600. &
- 1997. Why parent birds play favourites. Nature 390: 351–352. , , , &
- 2001. Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird the kittiwake Rissa tridactyla. Proc. R. Soc. Lond. B. 268: 647–650. , , &
- 1984. Why does the herring gull lay three eggs? Anim. Behav. 32: 798–805. , &
- 1998. A DNA test to sex most birds. Mol. Ecol. 7: 1071–1075. , , &
- 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal IgG transmission. Proc. R. Soc. Lond. B. 270: 2309–2319. , &
- 2002. The influence of laying sequence and habitat characteristics on maternal yolk hormone levels. Funct. Ecol. 16: 281–289. &
- 2005a. Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol. Lett. 1: 78–81. , , &
- 2005b. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29: 329–352. , , , &
- 1996. Effect of β-carotene, canthaxanthin, lutein and vitamin E on neonatal immunity of chicks when supplemented in broiler diets. Poult. Sci. 75: 1092–1097. , &
- 1999. Using Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. &
- 1999. Is avian humoral immunocompetence suppressed by testosterone? Behav. Ecol. Sociobiol. 45: 167–175. , , &
- 1976. Humoral immune response characteristics of testosterone-propionate-treated chickens. Immunology 30: 341–348. , , &
- 2004. Resistance of broiler chickens to Escherichia coli respiratory tract infection induced by passively transferred egg–yolk antibodies. Vet. Microbiol. 98: 273–284. , &
- 1999. Adaptation, exaptation, and constraint: a hormonal perspective. Am. Nat. 154: 4–25. &
- 1985. Quantitation of maternal–fetal IgG transport in the chicken. Immunology 54: 755–762. , , &
- 2000. Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Aegelius phoeniceus. Proc. R. Soc. Lond. B 267: 2005–2010. &
- 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88: 87–98. &
- 1991. Bird–Parasite Interactions. Oxford University Press, Oxford. &
- 1992. Neuroendocrine-immune interactions in the avian species – a review. Poult. Sci. Rev. 4: 129–167.
- 2003. Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am. Nat. 162: 704–712. &
- 1991. Variation in eggs and the period of rapid yolk deposition of the silver gull Larus Novaehollandiae during a protracted laying season. J. Zool. 223: 501–508.
- 1997. Why don't lay birds more eggs? TREE 12: 270–274. &
- 1998. The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc. R. Soc. Lond. B 265: 1731–1735. , &
- Mousseau, T.A. & Fox, C.W. (eds) 1998. Maternal Effects. Oxford University Press, New York.
- 2002. Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Gallus gallus domesticus). Proc. R. Soc. Lond. B 269: 2249–2256. , , &
- 2003. Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (Larus ridibundus) depend on the hatching order. Behav. Ecol. Sociobiol. 55: 80–86. , &
- 2004a. Within-clutch patterns of yolk testosterone vary with the onset of incubation in black-headed gulls. Behav. Ecol. 15: 893–897. , , &
- 2004b. Maternal antibody transmission and breeding densities in the black-headed gull (Larus ridibundus). Funct. Ecol. 18: 719–724. , , , &
- 2005. Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc. R. Soc. Lond. B., in press. , , , , &
- 1999. Experimental evidence that off spring sex ratio varies with maternal condition. Proc. Natl Acad. Sci. USA 96: 570–573. , , , &
- 2000. Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behav. Ecol. Sociobiol. 48: 452–457. , , &
- 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255–262. , , &
- 1975. Relationship between egg size and post-hatching chick mortality in the herring gull (Larus argentatus). Nature 228: 1221–1222.
- 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.
- 2001. Sex differences in avian yolk hormone levels. Nature 412: 498. , , &
- 2000. Multilevel Models Project. University of London, London. , , , &
- 1997. The relationship between gonadal steroids, immunocompetence, body mass, and behavior in young black-headed gulls (Larus ridibundus). Am. Nat. 150: 201–219. , &
- 2001. Maternal derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav. Ecol. 12: 381–385. , &
- 2003. Maternal IgG but not carotenoids in barn swallow eggs covary with embryo sex. J. Evol. Biol. 16: 516–522. , , , &
- 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B 266: 1–12. , , , &
- 1993. Yolk is a source of maternal testosterone for developing birds. Proc. Natl Acad. Sci. USA 90: 11446–11450.
- 1996. Maternal testosterone in the egg enhances postnatal growth. Comp. Biochem. Physiol. 114: 271–276.
- 1996. Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. TREE 11: 317–321. &
- 1999. Multilevel Analysis; An Introduction to Basic and Advanced Multilevel Modeling. Sage Publications, London. &
- 2000. Yolk androgens reduce offspring survival. Proc. R. Soc. Lond. B. 267: 1451–1456. &
- 2003. Trade-off between immunocompetence and growth in magpies: an experimental study. Proc. R. Soc. Lond. B 270: 241–248. , , , &
- 1995. Hatching asynchrony and the onset of incubation in birds, revisited: when is the critical period? In: Current Ornithology, Vol. 12 (D.M.Power, ed.), pp. 191–271. Plenum, New York. &
- 2002. Natural Antioxidants in Avian Nutrition and Reproduction. Nottingham University Press, Nottingham, UK.
- 1999. Tissue specific antioxidant profiles and susceptibility to lipid peroxidation of the newly hatched chick. Biol. Trace Elem. Res. 68: 63–78. , , &
- 2002. The evolutionary transition to coloniality promotes higher blood parasitism in birds. J. Evol. Biol. 15: 32–41.
- 2004. Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc. R. Soc. Lond. B 271: 1370–1375. , &
- 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 270: 2223–2232. , , , , , &
- 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506–513. , &
- 1987. Thermal tolerance of avian embryos: a review. Condor 89: 874–898.
- 1994. Intraspecific variation in egg size and egg composition in birds – effects on offspring fitness. Biol. Rev. 69: 35–59.