Long-lasting and sex-specific consequences of elevated egg yolk testosterone for social behavior in Japanese quail

Hormones and Behavior

Volumn 63, Issue 1, 2013, Pages 80-87

  Schweitzer, Cécile ^a   Goldstein, Michael H ^a   Place, Ned J ^a   Adkins Regan, Elizabeth ^a  

^a Cornell University ^*  (United States)

Author keywords

Birds; Maternal effects; Social behavior; Yolk testosterone

Indexed keywords

TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; COITUS; CONTROLLED STUDY; COTURNIX JAPONICA; EGG YOLK; EMBRYO; FEMALE; LIBIDO; MALE; MORPHOLOGICAL TRAIT; NONHUMAN; PRIORITY JOURNAL; QUAIL; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT; SOCIAL BEHAVIOR; TESTOSTERONE BLOOD LEVEL; VOCALIZATION;

ANIMALS; CHOICE BEHAVIOR; COTURNIX; EGG YOLK; FEMALE; MALE; SEX FACTORS; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; TESTOSTERONE;

EID: 84871931854     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.10.011     Document Type: Article

References (63)

1. Adkins E.K., Adler N.T. Hormonal control of behavior in the Japanese quail. J. Comp. Physiol. Psychol. 1972, 81:27-36.
2. Adkins-Regan E. Hormones and sexual differentiation of avian social behavior. Dev. Neurosci. 2009, 31:342-350.
3. Adkins-Regan E. Neuroendocrine contributions to sexual partner preference in birds. Front. Neuroendocrinol. 2011, 32:155-163.
4. Andersson S., Uller T., Lõhmus M., Sundström F. Effects of egg yolk testosterone on growth and immunity in a precocial bird. J. Evol. Biol. 2004, 17:501-505.
5. Arnqvist G., Kirkpatrick M. The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am. Nat. 2005, 165:S26-S37.
6. Ball G.F., Balthazart J. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol. Behav. 2004, 83:329-346.
7. Balthazart J., Ball G.F. Sexual differentiation of brain and behavior in birds. Trends Endocrinol. Metab. 1995, 6:21-29.
8. Balthazart J., Reid J., Absil P., Foidart A. Appetitive as well as consummatory aspects of male sexual behavior in quail are activated by androgens and estrogens. Behav. Neurosci. 1995, 109:485-501.
9. Balthazart J., Castagna C., Ball G.F. Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail. Behav. Neurosci. 1997, 111:381-397.
10. Beani L., Briganti F., Campanella G., Luo C., Dessì-Fulgheri F. Effect of androgens on structure and rate of crowing in the Japanese quail (Coturnix japonica). Behaviour 2000, 137:417-435.
11. Bertin A., Richard-Yris M.-A., Houdelier C., Lumineau S., Möstl E., Kuchar A., Hirschenhauser K., Kotrschal K. Habituation to humans affects yolk steroid levels and offspring phenotype in quail. Horm. Behav. 2008, 54:396-402.
12. Bertin A., Richard-Yris M.-A., Möstl E., Lickliter R. Increased yolk testosterone facilitates prenatal perceptual learning in Northern bobwhite quail (Colinus virginianus). Horm. Behav. 2009, 56:416-422.
13. Bolund E., Schielzeth H., Forstmeier W. Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males. Proc. R. Soc. B Biol. Sci. 2009, 276:707-715.
14. Bonisoli-Alquati A., Matteo A., Ambrosini R., Rubolini D., Romano M., Caprioli M., Dessì-Fulgheri F., Baratti M., Saino N. Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Horm. Behav. 2011, 59:75-82.
15. Carere C., Balthazart J. Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocrinol. Metab. 2007, 18:73-80.
16. Chiba A., Hosokawa N. Effects of androgens and estrogens on crowings and distress callings in male Japanese quail, Coturnix japonica. Horm. Behav. 2006, 49:4-14.
17. Cohen J. Statistical Power Analysis for the Behavioral Sciences 1988, Lawrence Earlbaum Associates, Hillsdale, NJ, USA. 2nd ed.
18. Daisley J.N., Bromundt V., Möstl E., Kotrschal K. Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica. Horm. Behav. 2005, 47:185-194.
19. Derégnaucourt S., Saar S., Gahr M. Dynamics of crowing development in the domestic Japanese quail (Coturnix coturnix japonica). Proc. R. Soc. Lond. B 2009, 276:2153-2162.
20. Eising C.M., Müller W., Groothuis T.G.G. Avian mothers create different phenotypes by hormone deposition in their eggs. Biol. Lett. 2006, 2:20-22.
21. Elf P.K., Fivizzani A.J. Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J. Exp. Zool. 2002, 293:594-600.
22. Fehér O., Wang H., Saar S., Mitra P.P., Tchernichovski O. De novo establishment of wild-type song culture in the zebra finch. Nature 2009, 459:564-568.
23. Forstmeier W., Martin K., Bolund E., Schielzeth H., Kempenaers B. Female extrapair mating behavior can evolve via indirect selection on males. Proc. Natl. Acad. Sci. 2011, 108:10608-10613.
24. Fritz C.O., Morris P.E., Richler J.J. Effect size estimates: current use, calculations, and interpretation. J. Exp. Psychol. Gen. 2012, 141:2-18.
25. Garcia-Fernandez V., Guasco B., Tanvez A., Lacroix A., Cucco M., Leboucher G., Malacarne G. Influence of mating preferences on yolk testosterone in the grey partridge. Anim. Behav. 2010, 80:45-49.
26. Gil D. Hormones in avian eggs: physiology, ecology and behavior. Adv. Study Behav. 2008, 38:337-398.
27. Gil D., Faure J.M. Correlated response in yolk testosterone levels following divergent selection for social behaviour in Japanese quail. J. Exp. Zool. 2007, 307A:91-94.
28. Gilbert L., Bulmer E., Arnold K.E., Graves J.A. Yolk androgens and embryo sex: maternal effects or confounding factors?. Horm. Behav. 2007, 51:231-238.
29. Glass G.V., Hopkins K.D. Statistical Methods in Education and Psychology 1984, Prentice-Hall, Inc., Englewood Cliffs, NJ, USA. 2nd ed.
30. Goodson J.L., Adkins-Regan E. Playback of crows of male Japanese quail elicits female phonotaxis. Condor 1997, 99:990-993.
31. Griffith S.C., Buchanan K.L. Maternal effects in the Zebra Finch: a model mother reviewed. Emu 2010, 110:251-267.
32. Groothuis T.G.G., Schwabl H. Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them?. Philos. Trans. R. Soc. B 2008, 363:1647-1661.
33. Groothuis T.G.G., Müller W., von Engelhardt N., Carere C., Eising C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 2005, 29:329-352.
34. Guyomarc'h J.C., Guyomarc'h C. Vocal communication in European quail; comparison with Japanese quail. C. R. Acad. Sci. Paris Life Sci. 1996, 319:827-834.
35. Guyomarc'h J.C., Aupiais A., Guyomarc'h C. Individual differences in the long-distance vocalizations used during pair bonding in European quail (Coturnix coturnix). Ethol. Ecol. Evol. 1998, 10:333-346.
36. Hackl R., Bromundt V., Daisley J., Kotrschal K., Möstl E. Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). J. Comp. Physiol. B 2003, 173:327-331.
37. Horváthová T., Nakagawa S., Uller T. Strategic female reproductive investment in response to male attractiveness in birds. Proc. R. Soc. B Biol. Sci. 2012, 279:163-170.
38. Kingma S.A., Komdeur J., Vedder O., von Engelhardt N., Korsten P., Groothuis T.G.G. Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition. Behav. Ecol. 2009, 20:172-179.
39. Koba N., Mori M., Ha Y., Mizushima S., Tsukada A., Saito N., Ono T., Shimada K. Effects of aromatase inhibitor (fadrozole)-induced sex-reversal on gonadal differentiation and mRNA expression of P450arom, AMH and ERα in embryos and growth in posthatching quail. J. Poult. Sci. 2008, 45:116-124.
40. Mateo J.M. Maternal influences on development, social relationships, and survival behaviors. Maternal Effects in Mammals 2009, The University of Chicago Press, Chicago, USA. D. Maestripieri, J.M. Mateo (Eds.).
41. Meddis R. Statistics Using Ranks: A Unified Approach 1984, Basil Blackwell, Oxford.
42. Mills A.D., Faure J.M. The treadmill test for the measurement of social motivation in Phasianidae chicks. Med. Sci. Res. 1990, 18:179-180.
43. Mousseau T.A., Fox C.W. The adaptive significance of maternal effects. Trends Ecol. Evol. 1998, 13:403-407.
44. Müller W., Groothuis T.G.G., Kasprzik A., Dijkstra C., Alatalo R.V., Siitari H. Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc. R. Soc. Lond. B 2005, 272:1971-1977.
45. Navara K.J., Hill G.E., Mendonça M.T. Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol. Biochem. Zool. 2005, 78:570-578.
46. Ottinger M.A., Brinkley H.J. Testosterone and sex related physical characteristics during the maturation of the male Japanese quail (Coturnix coturnix japonica). Biol. Reprod. 1979, 20:905-909.
47. Partecke J., Schwabl H. Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev. Neurobiol. 2008, 68:1538-1548.
48. Pilz K.M., Adkins-Regan E., Schwabl H. No sex difference in yolk concentrations of avian eggs at laying. Biol. Lett. 2005, 1:318-321.
49. Potash L.M. An experimental analysis of the use of location calls by japanese quail, Coturnix coturnix japonica. Behaviour 1975, 54:153-179.
50. Pryke S.R., Rollins L.A., Buttemer W.A., Griffith S.C. Maternal stress to partner quality is linked to adaptive offspring sex ratio adjustment. Behav. Ecol. 2011, 22:717-722.
51. Ramenofsky M. Agonistic behaviour and endogenous plasma hormones in male Japanese quail. Anim. Behav. 1984, 32:698-708.
52. Rubolini D., Romano M., Martinelli R., Saino N. Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav. Ecol. Sociobiol. 2006, 59:344-352.
53. Rubolini D., Martinelli R., von Engelhardt N., Romano M., Groothuis T.G.G., Fasola M., Saino N. Consequences of prenatal androgen exposure for the reproductive performance of female pheasants (Phasianus colchicus). Proc. R. Soc. Biol. Sci. Ser. B 2007, 274:137-142.
54. Ruuskanen S., Laaksonen T. Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca). Horm. Behav. 2010, 57:119-127.
55. Sachs B.D. Photoperiodic control of reproductive behavior and physiology of the male Japanese quail (Coturnix coturnix juponica). Horm. Behav. 1969, 1:7-24.
56. Schwabl H. Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11446-11450.
57. Schweitzer C., Poindron P., Arnould C. Social motivation affects the display of individual discrimination in young and adult japanese quail (Coturnix japonica). Dev. Psychobiol. 2009, 51:311-321.
58. Strasser R., Schwabl H. Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav. Ecol. Sociobiol. 2004, 56:491-497.
59. Tchernichovski O., Mitra P.P. Sound analysis Pro user manual http://soundanalysispro.com/.
60. Uller T., Eklöf J., Andersson S. Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behav. Ecol. Sociobiol. 2005, 57:584-590.
61. von Engelhardt N., Groothuis T.G.G. Maternal hormones in avian eggs. Hormones and Reproduction of Vertebrates, Volume 4-Birds 2011, Academic Press. D.O. Norris, K.H. Lopez (Eds.).
62. White D.J., Galef B.G. Affiliative preferences are stable and predict mate choices in both sexes of Japanese quail, Coturnix japonica. Anim. Behav. 1999, 58:865-871.
63. Yazaki Y., Matsushima T., Aoki K. Testosterone modulates stimulation-induced calling behavior in Japanese quails. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 1999, 184:13-19.