Yolk androgens and embryo sex: Maternal effects or confounding factors?

Hormones and Behavior

Volumn 51, Issue 2, 2007, Pages 231-238

  Gilbert, L ^a,b   Bulmer, E ^c   Arnold, K E ^d   Graves, J A ^b  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Albumin; Androgens; Egg; Embryo; Incubation; Sex; Taeniopygia guttata; Yolk; Zebra finch

Indexed keywords

ALBUMIN; ANDROGEN;

ANDROGEN METABOLISM; ANIMAL TISSUE; ARTICLE; CONFOUNDING VARIABLE; CONTROLLED STUDY; DILUTION; EGG; EGG YOLK; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; INCUBATION TIME; MOTHER; NONHUMAN; PRIORITY JOURNAL; PROGENY; SEX ALLOCATION; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; ZEBRA FISH;

ANIMALS; DIHYDROTESTOSTERONE; EGG YOLK; EMBRYO, NONMAMMALIAN; FEMALE; FINCHES; MALE; OVIPOSITION; SEX CHARACTERISTICS; SEX DIFFERENTIATION; TESTOSTERONE;

EID: 33846205102     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2006.10.005     Document Type: Article

References (46)

1. Adkins-Regan E., Abdelnabi M., Mobarak M., and Ottinger M.A. Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen. Comp. Endocrinol. 78 (1990) 93-109
2. Anderson D.J., Reeve J., and Bird D.M. Sexually dimorphic eggs, nestling growth and sibling competition in American kestrels, Falco sparverius. Funct. Ecol. 11 (1997) 331-335
3. Arnold K.E., Orr K.J., and Griffiths R. Primary sex ratios in birds: problems with molecular sex identification of undeveloped eggs. Mol. Ecol. 12 (2003) 3451-3458
4. Badyaev A.V., Schwabl H., Young R.L., Duckworth R.A., Navara K.J., and Parlow A.F. Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird. Proc. R. Soc. London, Ser. B Biol. Sci. 272 (2005) 2165-2172
5. Balzer A.L., and Williams T.D. Do female Zebra Finches vary in primary reproductive effort in relation to mate attractiveness?. Behaviour 135 (1998) 297-309
6. Burley N. The differential-allocation hypothesis-an experimental test. Am. Nat. 132 (1988) 611-628
7. Cordero P.J., Griffith S.C., Aparicio J.M., and Parkin D.T. Sexual dimorphism in house sparrow eggs. Behav. Ecol. Sociobiol. 48 (2000) 353-357
8. Cordero P.J., Vinuela J., Aparicio J.M., and Veiga J.P. Seasonal variation in sex ratio and sexual egg dimorphism favours daughters in first clutches of the spotless starling. J. Evol. Biol. 14 (2001) 829-834
9. Cunningham E.J.A., and Russell A.F. Egg investment is influenced by male attractiveness in the mallard. Nature 404 (2000) 74-76
10. de Lope F., and Møller A.P. Female reproductive effort depends on the degree of ornamentation of their mates. Evolution 47 (1993) 1152-1160
11. Eising C.M., Eikenaar C., Schwabl H., and Groothuis T.G.G. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc. R. Soc. London, Ser. B Biol. Sci. 268 (2001) 839-846
12. Eising C.M., Müller W., Dijkstra C., and Groothuis T.G.G. Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen. Comp. Endocrinol. 132 (2003) 241-247
13. Elf P.K., and Fivizzani A.J. Changes in sex steroid levels in yolks of the Leghorn chicken, Gallus domesticus, during embryonic development. J. Exp. Zool. 293 (2002) 594-600
14. Gil D., Graves J.A., Hazon N., and Wells A. Male attractiveness and differential testosterone investment in zebra finch eggs. Science 268 (1999) 126-128
15. Gil D., Leboucher G., Lacroix A., Cue R., and Kreutzer M. Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm. Behav. 45 (2004) 64-70
16. Gilbert L., Rutstein A.N., Hazon N., and Graves J.A. Sex-biased investment in yolk androgens depends on female quality and laying order in zebra finches (Taeniopygia guttata). Naturwissenschaften 92 (2005) 178-181 10.1007/s00114-004-0603-z
17. Gilbert L., Williamson K.A., Hazon N., and Graves J.A. Maternal effects due to male attractiveness affect offspring fitness in the zebra finch. Proc. R. Soc. London, Ser. B Biol. Sci. (2006) 10.1098/rspb.2006.3520
18. Gorman H.E., and Nager R.G. State-dependent incubation behaviour in the zebra finch. Anim. Behav. 65 (2003) 745-754
19. Gorman H.E., and Nager R.G. Prenatal developmental conditions have long-term effects on offspring fecundity. Proc. R. Soc. London, Ser. B Biol. Sci. 271 (2004) 1923-1928
20. Gorman H.E., Orr K.J., Adam A., and Nager R.G. Effects of incubation conditions and offspring sex on embryonic development and survival in the zebra finch (Taeniopygia guttata). Auk 122 (2005) 1239-1248
21. Grafen A., and Hails R. Modern Statistics for the Life Sciences (2002), Oxford Univ. Press. 0-19-925231-9
22. Griffiths R., Double M.C., Orr K., and Dawson R.J.G. A DNA test to sex most birds. Mol. Ecol. 7 (1998) 1071-1075
23. Groothuis T.G.G., and von Engelhardt N. Investigating maternal hormones in avian eggs: measurement, manipulation and interpretation. Ann. N. Y. Acad. Sci. 1046 (2005) 168-180
24. Groothuis T.G.G., Müller W., von Engelhardt N., Carere C., and Eising C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29 (2005) 329-352 10.1016/j.neubiorev.2004.12.002
25. Magrath M.J.L., Brouwer L., and Komdeur J. Egg size and laying order in relation to offspring sex in the extreme sexually size dimorphic brown songlark, Cinclorhamphus cruralis. Behav. Ecol. Sociobiol. 54 (2003) 240-248
26. Martins T.L.F. Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment. Behav. Ecol. 15 (2004) 174-180
27. Mead P.S., Morton M.L., and Fish B.E. Sexual dimorphism in egg size and implications regarding facultative manipulation of sex in mountain white-crowned sparrows. Condor 89 (1987) 798-803
28. Mousseau T.A., and Fox C.W. The adaptive significance of maternal effects. Trends Ecol. Evol. 13 (1998) 403-407
29. Müller W., Eising C.M., Dijkstra C., and Groothuis T.G.G. Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Gallus gallus domesticus). Proc. R. Soc. London, Ser. B Biol. Sci. 269 (2002) 2249-2255
30. Müller W., Groothuis T.G.G., Eising C.M., Daan S., and Dijkstra C. Within clutch co-variation of egg mass and sex in the black-headed gull. J. Evol. Biol. 18 (2005) 661-668
31. Nash J.P., Cuisset B.D., Bhattacharyya S., Suter H.C., Le Menn F., and Kime D.E. An enzyme linked immunosorbant assay (ELISA) for testosterone, estradiol, and 17,20 beta-dihydroxy-4-pregenen-3-one using acetylcholinesterase as tracer: application to measurement of diel patterns in rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 22 (2000) 355-363
32. Petrie M., and Williams W.A. Peahens lay more eggs for peacocks with larger trains. Proc. R. Soc. London, Ser. B Biol. Sci. 251 (1993) 127-131
33. Rubolini D., Romano M., Martinelli R., Leoni B., and Saino N. Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav. Ecol. Sociobiol. 59 (2006) 549-560
34. Rutkowska J., and Cichon M. Maternal investment during egg laying and offspring sex: an experimental study of zebra finches. Anim. Behav. 64 (2002) 817-822
35. Rutstein A.N., Gilbert L., Slater P.J.B., and Graves J.A. Mate attractiveness and primary resource allocation in the zebra finch. Anim. Behav. 68 (2004) 1087-1094
36. Rutstein A.N., Slater P.J.B., and Graves J.A. Diet quality and resource allocation in the zebra finch. Proc. R. Soc., B 271 S5 (2004) 286-289 10.1098/rsbl.2003.0154
37. Rutstein A.N., Gilbert L., Slater P.J.B., and Graves J.A. Sex-specific patterns of yolk androgen allocation depend on maternal diet in the zebra finch. Behav. Ecol. 16 (2005) 62-69
38. Rutstein A.N., Gorman H.E., Arnold K.E., Gilbert L., Orr K.J., Adam A., Nager R., and Graves J.A. Sex allocation in response to paternal attractiveness in the zebra finch. Behav. Ecol. 16 (2005) 763-769
39. Saino N., Ferrari R.P., Martinelli R., Romano M., Rubolini D., and Møller A.P. Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc. R. Soc. London, Ser. B Biol. Sci. 269 (2002) 1005-1009
40. Sockman K.W., and Schwabl H. Yolk androgens reduce offspring survival. Proc. R. Soc. London, Ser. B Biol. Sci. 267 (2000) 1451-1456
41. Trivers R.L., and Willard D.E. Natural selection of parental ability to vary the sex ratio of the offspring. Science 179 (1973) 90-92
42. Uller T., Eklöf J., and Andersson S. Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behav. Ecol. Sociobiol. 57 (2005) 584-590
43. von Engelhardt N., and Groothuis T.G.G. Measuring steroid hormones in avian eggs. Ann. N. Y. Acad. Sci. 1046 (2005) 181-192
44. von Engelhardt N., Carere C., Dijkstra C., and Groothuis T.G.G. Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc. R. Soc. London, Ser. B Biol. Sci. 273 (2006) 65-70
45. Williamson K.A., Surai F.P., and Graves J.A. Yolk antioxidants and mate attractiveness in the zebra finch. Funct. Ecol. 20 (2006) 354-359
46. Young R.L., and Badyaev A.V. Evolution of sex-biased maternal effects in birds: 1. Sex-specific resource allocation among simultaneously growing oocytes. J. Evol. Biol. 17 (2004) 1355-1366