Growth and innate immunity are not limited by selection for high egg testosterone content in Japanese quail

Journal of Experimental Biology

Volumn 215, Issue 4, 2012, Pages 617-622

  Kankova, Zuzana ^a   Zeman, Michal ^a,b   Okuliarova, Monika ^a  

^a Physics and Informatics   (Slovakia)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Corticosterone; Growth; Innate immunity; Plasma antibodies; Yolk androgens

Indexed keywords

CORTICOSTERONE; EGG PROTEIN; IMMUNOGLOBULIN; IMMUNOGLOBULIN Y; TESTOSTERONE;

ANIMAL; ARTICLE; BLOOD; COTURNIX; EGG; EGG YOLK; FEMALE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; MALE; PHYSIOLOGY;

ANIMALS; CORTICOSTERONE; COTURNIX; EGG PROTEINS; EGG YOLK; EGGS; FEMALE; IMMUNITY, INNATE; IMMUNOGLOBULINS; MALE; TESTOSTERONE;

COTURNIX JAPONICA; PHASIANIDAE;

EID: 84856549212     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.064030     Document Type: Article

References (55)

1. Andersson, S., Uller, T., Lohmus, M. and Sundstrom, F. (2004). Effects of egg yolk testosterone on growth and immunity in a precocial bird. J. Evol. Biol. 17, 501-505. (Pubitemid 38571946)
2. Apanius, V. (1998). Stress and immune defense. Stress Behav. 27, 133-153.
3. Baumann, H. and Gauldie, J. (1994). The acute-phase response. Immunol. Today 15, 74-80.
4. Brambell, F. W. R. (1970). The transmission of passive immunity from mother to young. Amsterdam: North-Holland Publishing Co.
5. Brzȩk, P. and Konarzewski, M. (2007). Relationship between avian growth rate and immune response depends on food availability. J. Exp. Biol. 210, 2361-2367. (Pubitemid 47080214)
6. Cucco, M., Guasco, B., Malacarne, G., Ottonelli, R. and Tanvez, A. (2008). Yolk testosterone levels and dietary carotenoids influence growth and immunity of grey partridge chicks. Gen. Comp. Endocrinol. 156, 418-425.
7. Dhabhar, F. S. (2009). Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulation 16, 300-317.
8. Eising, C. M. and Groothuis, T. G. G. (2003). Yolk androgens and begging behaviour in black-headed gull chicks: An experimental field study. Anim. Behav. 66, 1027-1034. (Pubitemid 38033713)
9. Eising, C. M., Müller, W. and Groothuis, T. G. G. (2006). Avian mothers create different phenotypes by hormone deposition in their eggs. Biol. Lett. 2, 20-22. (Pubitemid 43384662)
10. Gasc, J. M. and Stumpf, W. E. (1981). The bursa of Fabricius of the chicken embryo: Localization and ontogenic evolution of sex-steroid target cells. J. Embryol. Exp. Morphol. 63, 225-231. (Pubitemid 11072257)
11. Gasparini, J., McCoy, K. D., Staszewski, V., Haussy, C. and Boulinier, T. (2006). Dynamics of anti-Borrelia antibodies in blacklegged kittiwake (Rissa tridactyla) chicks suggest a maternal educational effect. Can. J. Zool. 84, 623-627. (Pubitemid 44049538)
12. Gil, D. (2008). Hormones in avian eggs: Physiology, ecology and behavior. Adv. Stud. Behav. 38, 337-398.
13. Grindstaff, J. L. (2008). Maternal antibodies reduce costs of an immune response during development. J. Exp. Biol. 211, 654-660. (Pubitemid 351551794)
14. Grindstaff, J. L. (2010). Initial levels of maternally derived antibodies predict persistence time in offspring circulation. J. Ornithol. 151, 423-428.
15. Grindstaff, J. L., Demas, G. E. and 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. (Pubitemid 44929389)
16. Groothuis, T. G. G. and Schwabl, H. (2008). Hormone-mediated maternal effects in birds: Mechanisms matter but what do we know of them? Philos. Trans. R. Soc. Lond. B 363, 1647-1661. (Pubitemid 351441048)
17. Groothuis, T. G. G., Eising, C. M., Dijkstra, C. and Müller, W. (2005a). Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol. Lett. 1, 78-81. (Pubitemid 41529989)
18. Groothuis, T. G. G., Müller, W., von Engelhardt, N., Carere, C. and Eising, C. (2005b). Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29, 329-352. (Pubitemid 40461749)
19. Harmon, B. G. (1998). Avian heterophils in inflammation and disease resistance. Poult. Sci. 77, 972-977. (Pubitemid 128525109)
20. Hegyi, G. and Schwabl, H. (2010). Do different yolk androgens exert similar effects on the morphology or behaviour of Japanese quail hatchlings Coturnix japonica? J. Avian Biol. 41, 258-265.
21. Jensen, L. E. and Whitehead, A. S. (1998). Regulation of serum amyloid A protein expression during the acute-phase response. Biochem. J. 334, 489-503. (Pubitemid 28457193)
22. Kincade, P. W. and Cooper, M. D. (1971). Development and distribution of immunoglobulin-containing cells in the chicken. An immunofluorescent analysis using purified antibodies to mu, gamma and light chains. J. Immunol. 106, 371-382.
23. Klasing, K. C. (2004). The cost of immunity. Acta Zool. Sinica 50, 961-969.
24. Koutsos, E. A. and Klasing, K. C. (2001). The acute phase response in Japanese quail (Coturnix coturnix japonica). Comp. Biochem. Physiol. 128C, 255-263. (Pubitemid 32402195)
25. Leshchinsky, T. V. and Klasing, K. C. (2001). Divergence of the inflammatory response in two types of chickens. Dev. Comp. Immunol. 25, 629-638. (Pubitemid 32694671)
26. Mast, J. and Goddeeris, B. M. (1999). Development of immunocompetence of broiler chickens. Vet. Immunol. Immunopathol. 70, 245-256. (Pubitemid 29460875)
27. Mousseau, T. A. and Fox, C. W. (1998). The adaptive significance of maternal effects. Trends Ecol. Evol. 13, 403-407. (Pubitemid 28430680)
28. Müller, W., Groothuis, T. G. G., Kasprzik, A., Dijkstra, C., Alatalo, R. V. and Siitari, H. (2005). Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc. R. Soc. Lond. B 272, 1971-1977. (Pubitemid 41414650)
29. Müller, W., Vergauwen, J. and Eens, M. (2008). Yolk testosterone, postnatal growth and song in male canaries. Horm. Behav. 54, 125-133.
30. Müller, W., Dijkstra, C. and Groothuis, T. G. G. (2009). Maternal yolk androgens stimulate territorial behaviour in black-headed gull chicks. Biol. Lett. 5, 586-588.
31. Nakamura, K., Mitarai, Y., Yoshioka, M., Koizumi, N., Shibahara, T. and Nakajima, Y. (1998). Serum levels of interleukin-6, alpha1-acid glycoprotein, and corticosterone in two-week-old chickens inoculated with Escherichia coli lipopolysaccharide. Poult. Sci. 77, 908-911. (Pubitemid 128525144)
32. Navara, K. J., Hill, G. E. and Mendonca, M. T. (2005). Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol. Biochem. Zool. 78, 570-578. (Pubitemid 40870441)
33. Navara, K. J., Hill, G. E. and Mendonca, M. T. (2006). Yolk testosterone stimulates growth and immunity in house finch chicks. Physiol. Biochem. Zool. 79, 550-555. (Pubitemid 43846270)
34. Norton, J. M. and Wira, C. R. (1977). Dose-related effects of the sex hormones and cortisol on the growth of the bursa of Fabricius in chick embryos. J. Steroid Biochem. 8, 985-987. (Pubitemid 8174755)
35. Okuliarova, M., Kostal, L. and Zeman, M. (2011a). Effects of divergent selection for yolk testosterone content on growth characteristics of Japanese quail. Comp. Biochem. Physiol. 160A, 81-86.
36. Okuliarova, M., Groothuis, T. G. G., Skrobanek, P. and Zeman, M. (2011b). Experimental evidence for genetic heritability of maternal hormone transfer to offspring. Am. Nat. 177, 824-834.
37. Owen-Ashley, N. T. and Wingfield, J. C. (2007). Acute phase responses of passerine birds: Characterization and seasonal variation. J. Ornithol. 148, S583-S591. (Pubitemid 350238511)
38. Partecke, J. and Schwabl, H. (2008). Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev. Neurobiol. 68, 1538-1548.
39. Pitala, N., Ruuskanen, S., Laaksonen, T., Doligez, B., Tschirren, B. and Gustafsson, L. (2009). The effects of experimentally manipulated yolk androgens on growth and immune function of male and female nestling collared flycatchers Ficedula albicollis. J. Avian Biol. 40, 225-230.
40. Reid, J. M., Arcese, P., Keller, L. F. and Hasselquist, D. (2006). Long-term maternal effect on offspring immune response in song sparrows Melospiza melodia. Biol. Lett. 2, 573-576. (Pubitemid 44935434)
41. Rubolini, D., Romano, M., Martinelli, R., Leoni, B. and Saino, N. (2006). Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav. Ecol. Sociobiol. 59, 549-560. (Pubitemid 43117664)
42. Saino, N., Ferrari, R. P., Romano, M., Martinelli, R., Lacroix, A., Gil, D. and Moller, A. P. (2006). Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters. Behav. Ecol. 17, 172-181. (Pubitemid 43209186)
43. Sandell, M. I., Tobler, M. and Hasselquist, D. (2009). Yolk androgens and the development of avian immunity: An experiment in jackdaws (Corvus monedula). J. Exp. Biol. 212, 815-822.
44. Sapolsky, R. M., Romero, L. M. and Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55-89. (Pubitemid 32266068)
45. Schwabl, H. (1996). Maternal testosterone in the avian egg enhances postnatal growth. Comp. Biochem. Physiol. 114A, 271-276. (Pubitemid 26234068)
46. Shini, S., Kaiser, P., Shini, A. and Bryden, W. L. (2008a). Biological response of chickens (Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comp. Biochem. Physiol. 149B, 324-333. (Pubitemid 350300013)
47. Shini, S., Kaiser, P., Shini, A. and Bryden, W. L. (2008b). Differential alterations in ultrastructural morphology of chicken heterophils and lymphocytes induced by corticosterone and lipopolysaccharide. Vet. Immunol. Immunopathol. 122, 83-93. (Pubitemid 351273816)
48. Sockman, K. W. and Schwabl, H. (2001). Plasma corticosterone in nestling American kestrels: Effects of age, handling stress, yolk androgens, and body condition. Gen. Comp. Endocrinol. 122, 205-212. (Pubitemid 32424197)
49. Sockman, K. W., Weiss, J., Webster, M. S., Talbott, V. and Schwabl, H. (2008). Sex-specific effects of yolk-androgens on growth of nestling American kestrels. Behav. Ecol. Sociobiol. 62, 617-625.
50. Soler, J. J., de Neve, L., Perez-Contreras, T., Soler, M. and Sorci, G. (2003). Tradeoff between immunocompetence and growth in magpies: An experimental study. Proc. R. Soc. Lond. B 270, 241-248. (Pubitemid 36228526)
51. Tobler, M., Hasselquist, D., Smith, H. G. and Sandell, M. I. (2010). Short- and longterm consequences of prenatal testosterone for immune function: An experimental study in the zebra finch. Behav. Ecol. Sociobiol. 64, 717-727.
52. Trout, J. M., Mashaly, M. M. and Siegel, H. S. (1996). Changes in blood and spleen lymphocyte populations following antigen challenge in immature male chickens. Br. Poult. Sci. 37, 819-827. (Pubitemid 126463737)
53. Tschirren, B., Saladin, V., Fitze, P. S., Schwabl, H. and Richner, H. (2005). Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J. Anim. Ecol. 74, 675-682. (Pubitemid 41576935)
54. von Engelhardt, N., Carere, C., Dijkstra, C. and Groothuis, T. G. G. (2006). Sexspecific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc. R. Soc. Lond. B 273, 65-70. (Pubitemid 46768046)
55. Watanabe, S. and Nagayama, F. (1979). Studies on the serum IgG level in Japanese quail. Jpn. Poult. Sci. 16, 59-64.