Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird

Journal of Evolutionary Biology

Volumn 20, Issue 3, 2007, Pages 874-880

  Gasparini, Julien ^a   Boulinier, T ^b   Gill, V A ^c,d   Gil, D ^e   Hatch, S A ^c   Roulin, A ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^c U S GEOLOGICAL SURVEY   (United States)

^d U S FISH AND WILDLIFE SERVICE   (United States)

^e MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Immunoglobulins; Kittiwake; Maternal effects; Replacement Clutch; Testoterone

Indexed keywords

ANDROGEN; ANTIBODY;

ANDROGEN; ANTIBODY; COLONIAL ORGANISM; EGG; EGG PRODUCTION; FOOD AVAILABILITY; MATERNAL EFFECT; REPRODUCTION; REPRODUCTIVE EFFORT; SEABIRD;

ANIMAL; ARTICLE; CHARADRIIFORMES; CLUTCH SIZE; FEEDING BEHAVIOR; FEMALE; MATERNAL BEHAVIOR; METABOLISM; NESTING; OOCYTE; PHYSIOLOGY;

ANDROGENS; ANIMALS; ANTIBODIES; CHARADRIIFORMES; CLUTCH SIZE; FEEDING BEHAVIOR; FEMALE; MATERNAL BEHAVIOR; NESTING BEHAVIOR; OVUM;

RISSA TRIDACTYLA;

EID: 34247515919     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2007.01315.x     Document Type: Article

References (35)

1. Agrawal, A.A. 2001. Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect. Am. Nat. 157: 555-569.
2. Badzinski, S.S., Ankney, C.D., Leafloor, J.O. & Abraham, K.F. 2002. Egg size as a predictor of nutrient composition of eggs and neonates of Canada geese (Branta canadensis interior) and Lesser Snow Geese (Chen caerulescens caerulescens). Can. J. Zool. 80: 333-341.
3. Bernardo, J. 1996. Maternal effects in animal ecology. Am. Zool. 36: 83-105.
4. 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, Biol. Sci. 269: 29-36.
5. Coulson, J.C. 1963. Egg size and shape in the kittiwake (Rissa tridactyla) and their use in estimating age composition of populations. Proc. Zool. Soc. Lond. 140: 211-227.
6. Crowther, J.R. 2001. The Elisa guidebook. Methods in Molecular Biology, Vol. 149. Humana Press, Totowa, NJ.
7. De Neve, L., Soler, J.J., Soler, M. & Pérez-Contreras, T. 2004. Differential investment counteracts for late breeding in magpies Pica pica: an experimental study. J. Avian Biol. 35: 237-345.
8. Gasparini, J., McCoy, K.D., Haussy, C., Tveraa, T. & Boulinier, T. 2001. Induced maternal response to the Lyme disease spirochete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc. R. Soc. Lond., B, Biol. Sci. 268: 647-650.
9. Gasparini, J., McCoy, K.D., Tveraa, T. & Boulinier, T. 2002. Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecol. Lett. 5: 519-524.
10. Gasparini, J., Roulin, A., Gill, V.A., Hatch, S.A. & Boulinier, T. 2006a. Kittiwakes strategically reduce investment in replacement clutches. Proc. R. Soc. Lond., B, Biol. Sci. 273: 1550-1554.
11. Gasparini, J., Roulin, A., Gill, V.A., Hatch, S.A. & Boulinier, T. 2006b. In kittiwakes food availability partially explains the seasonal decline in humoral immunocompetence. Funct. Ecol. 20: 457-463.
12. Gil, D., Heim, C., Bulmer, E., Rocha, M., Puerta, M. & Naguib, M. 2004. Negative effects of early developmental stress on yolk testosterone levels in a passerine bird. J. Exp. Biol. 207: 2215-2220.
13. Gill, V.A., Hatch, S.A. & Lanctot, R.B. 2004. Colonization, population growth and nesting success of black oystercatchers following a seismic uplift. Condor 106: 791-800.
14. Gorman, H.E. & Nager, R.G. 2004. Prenatal developmental conditions have long-term effects on offspring fecundity. Proc. R. Soc. Lond., B, Biol. Sci. 271: 1923-1928.
15. Grindstaff, J.L., Brodie, E.D., III & Ketterson, E.D. 2003. Immune functions across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. R. Soc. Lond., B, Biol. Sci. 270: 2309-2319.
16. Grindstaff, J.L., Demas, G.E. & Ketterson, E.D. 2005. Diet quality affects egg size and number but does not reduce maternal antibody transmission in Japanese quail Coturnix japonica. J. Anim. Ecol. 74: 1051-1058.
17. Groothuis, T.G.G., Müller, W., von Engelhardt, N., Carere, C. & Eising, C. 2005. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29: 329-352.
18. Groothuis, T.G.G., Eising, C.M., Blount, J.D., Surai, P., Apanius, V., Dijkstra, C. & Müller, W. 2006. Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J. Evol. Biol. 19: 1304-1313.
19. Hargitai, R., Prechl, J. & Török, J. 2006. Maternal immunoglobulin concentration in Collared Flycatcher (Ficedula albicolis) eggs in relation to parental quality and laying order. Funct. Ecol. 20: 829-838.
20. Klasing, K.C. 1998. Nutritional modulation of resistance to infectious diseases. Poult. Sci. 77: 119-1125.
21. Littell, R.C., Milliken, G.A., Stroup, W.W. & Wolfinger, R.D. 1996. SAS System for Mixed Models. SAS Institute, Cary, NC.
22. Martinez, J., Tomás, G., Merino, S., Arriero, E. & Moreno, J. 2003. Detection of serum immunoglobulins in wild birds by direct ELISA: a methodological study to validate the technique in different species using antichicken antibodies. Funct. Ecol. 17: 700-706.
23. Mohammed, H.O., Yamamoto, R., Carpenter, T.E. & Ortmayer, H.B. 1986. Comparison of egg yolk and serum for the detection of Mycoplasma gallisepticum and M. synoviae antibodies by enzyme-linked immunosorbent assays. Avian Dis. 30: 398-408.
24. Mondal, S.P. & Naqi, S.A. 2001Maternal antibody to infectious bronchitis virus: its role in protection against infection and development of active immunity to vaccine. Vet. Immunol. Immunopathol. 79: 31-40.
25. Moreno, J. 1998. The determination of seasonal declines in breeding success in seabirds. Etología 6: 17-31.
26. Mousseau, T.A. & Fox, C.W. 1998. Maternal Effects as Adaptations. Oxford University Press, Oxford.
27. Müller, W., Groothuis, T.G.G., Kasprzik, A., Dijkstra, C., Alatalo, R.V. & Siitari, H. 2005. Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Funct. Ecol. 18: 719-724.
28. Naguib, M. & Gil, D. 2005. Transgenerational body size effects caused by early developmental stress in zebra finches. Biol. Lett. 1: 95-97.
29. Oro, D. & Furness, R.W. 2002. Influences of food availability and predation on survival of kittiwakes. Ecology 83: 2516-2528.
30. Pastoret, P., Gabriel, P., Bazin, H. & Govaerts, A. 1998. Handbook of Vertebrate Immunology. Academic Press, San Diego, CA.
31. Rubolini, D., Romano, M., Martinelli, R., Leoni, B. & Saino, N. 2006. Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav. Ecol. Sociobiol. 59: 549-560.
32. SAS 1996. SAS, User's Manual. SAS Institute Inc., Cary, NC.
33. Siegrist, C.A. 2003. Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypothesesand definition of main determinants. Vaccine 21: 3406-3412.
34. Uller, T., Eklöf, J. & Andersson, S. 2005. Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behav. Ecol. Sociobiol. 57: 584-590.
35. Verboven, N., Monaghan, P., Evans, D.M., Schwabl, H., Evans, N., Whitelaw, C. & Nager, R.G. 2003. Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser back-backed gull (Larus fuscus). Proc. R. Soc. Lond., B, Biol. Sci. 270: 2223-2232.