Mind the gap: The ratio of yolk androgens and antioxidants varies between sons and daughters dependent on paternal attractiveness

Behavioral Ecology and Sociobiology

Volumn 66, Issue 4, 2012, Pages 519-527

  Pariser, E C ^a   Gilbert, L ^b   Hazon, N ^a   Arnold, K E ^c   Graves, J A ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Androgens; Antioxidants; Maternal effects; Sex ratio; Zebra finch

Indexed keywords

ANTIOXIDANT; CLUTCH SIZE; FITNESS; MATERNAL EFFECT; PARENTAL INVESTMENT; PASSERINE; RESOURCE ALLOCATION; SEX RATIO;

TAENIOPYGIA GUTTATA;

EID: 84858157295     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-011-1300-5     Document Type: Article

References (58)

1. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 7: 363-368.
2. Birkhead TR, Hunter FM, Pellatt JE (1989) Sperm competition in the zebra finch, Taeniopygia-guttata. Anim Behav 38: 935-950. doi: 10. 1016/s0003-3472(89)80135-6.
3. Birkhead TR, Burke T, Zann R, Hunter FM, Krupa AP (1990) Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata, revealed by DNA fingerprinting. Behav Ecol Sociobiol 27: 315-324.
4. Blount JD, Houston DC, Surai PF, Møller AP (2004) Egg-laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proc R Soc Lond B 271: S79-S81.
5. Bolund E, Schielzeth H, Forstmeier W (2009) Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males. Proc R Soc Lond B 276: 707-715.
6. Boncoraglio G, Groothuis TGG, von Engelhardt N (2011) Differential maternal testosterone allocation among siblings benefits both mother and offspring in the zebra finch Taeniopygia guttata. Am Nat 178: 64-74.
7. Burley N (1981) Sex ratio manipulation and selection for attractiveness. Science 211: 721-722.
8. Burley N (1986) Sex-ratio manipulation in color-banded populations of zebra finches. Evolution 40: 1191-1206.
9. Burley N (1988) The differential-allocation hypothesis: an experimental test. Am Nat 132: 611-628.
10. Cucco M, Guasco B, Malacarne G, Ottonelli R, Tanvez A (2008) Yolk testosterone levels and dietary carotenoids influence growth and immunity of grey partridge chicks. Gen Comp Endocrinol 156: 418-425.
11. Cunningham EJA, Russell A (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404: 74-77.
12. Duffy DL, Bentley GE, Drazen DL, Ball GF (2000) Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav Ecol 11: 654-662.
13. Eising CM, Groothuis TGG (2003) Yolk androgens and begging behaviour in black-backed gull chicks: an experimental field study. Anim Behav 66: 1027-1034.
14. Gil D (2008) Hormones in avian eggs: a review. Adv Study Behav 38: 337-398.
15. Gil D, Graves J, HazonN WA (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286: 126-128.
16. Gil D, Leboucher G, Lacroix A, Cue R, Kreutzer M (2004) Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav 45: 64-70.
17. Gilbert L, Rutstein AN, Hazon N, Graves JA (2005) Sex-biased investment in yolk androgens depends on female quality and laying order in zebra finches (Taeniopygia guttata). Naturwissenschaften 92: 178-181.
18. Gilbert L, Williamson KA, Hazon N, Graves JA (2006) Maternal effects due to male attractiveness affect offspring development in the zebra finch. Proc R Soc Lond B 273: 1765-1771.
19. Gilbert L, Bulmer E, Arnold KE, Graves JA (2007) Yolk androgens and embryo sex: maternal effects or confounding factors? Horm Behav 51: 231-238.
20. Gilbert L, Williamson KA, Graves JA (2011) Male attractiveness regulates offspring fecundity non-genetically via maternal investment. Proc R Soc Lond B. doi: 10. 1098/rspb. 2011. 0962.
21. Gowaty PA, Anderson WW, Bluhm CK, Drickamer LC, Kim YK, Moore AJ (2007) The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Natl Acad Sci USA 104: 15023-15027.
22. Griffith SC, Holleley CE, Mariette MM, Pryke SR, Svedin N (2010) Low level of extra pair parentage in wild zebra finches. Anim Behav 79: 261-264.
23. Groothuis TGG, Muller 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.
24. Groothuis TGG, Eising CM, Blount JD, Surai P, Apanius V, Dijkstra C, Muller W (2006) Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J Evol Biol 19: 1304-1313.
25. Hargitai R, Arnold KE, Herenyi M, Prechl J, Torok J (2009) Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav Ecol Sociobiol 63: 869-882.
26. Harris WE, Uller T (2009) Reproductive investment when mate quality varies: differential allocation versus reproductive compensation. Phil Trans R Soc B-Bio Sci 364: 1039-1048.
27. Hunt S, Cuthill IC, Swaddle JP, Bennett ATD (1997) Ultraviolet vision and band-colour preferences in female zebra finches, Taeniopygia guttata. Anim Behav 54: 1383-1392.
28. Ketterson ED, Nolan V (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154: S4-S25.
29. Kilner R (1998) Primary and secondary sex ratio manipulation by zebra finches. Anim Behav 56: 155-164.
30. Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B 267: 2005-2010.
31. Martins TLF (2004) Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment. Behav Ecol 15: 174-180.
32. Monaghan P, Nager RG (1997) Why don't birds lay more eggs? Trends Ecol Evol 12: 270-274.
33. Müller W, Boonen S, Groothuis TGG, Eens M (2010) Maternal yolk testosterone in canary eggs: toward a better understanding of mechanisms and function. Behav Ecol 21: 493-500.
34. Navara KJ, Hill GE, Mendonca MT (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol Biochem Zool 78: 570-578.
35. Navara KJ, Hill GE, Medonca MT (2006a) Yolk androgen deposition as a compensatory strategy. Behav Ecol Sociobiol 60: 392-398.
36. Navara KJ, Badyaev AV, Mendonca MT, Hill GE (2006b) Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiol Biochem Zool 79: 1098-1105.
37. Petrie M, Williams A (1993) Peahens lay more eggs for peacocks with larger trains. Proc R Soc Lond B 251: 127-131.
38. Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12: 381-385.
39. Rutstein AN, Gilbert L, Slater PJB, Graves JA (2004a) Mate attractiveness and primary resource allocation in the zebra finch. Anim Behav 68: 1087-1094.
40. Rutstein AN, Slater PJB, Graves JA (2004b) Diet quality and resource allocation in the zebra finch. Proc R Soc Lond B 271: S286-S289.
41. Rutstein AN, Gilbert L, Slater PJB, Graves JA (2005a) Sex-specific patterns of yolk androgen allocation depend on maternal diet in the zebra finch. Behav Ecol 16: 62-69.
42. Rutstein AN, Gorman HE, Arnold KE, Gilbert L, Orr KJ, Adam A, Nager R, Graves JA (2005b) Sex allocation in response to paternal attractiveness in the zebra finch. Behav Ecol 16: 763-769.
43. Safran R, Pilz K, McGraw K, Correa S, Schwabl H (2008) Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behav Ecol Sociobiol 62: 427-438.
44. Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B: 269: 1729-1733.
45. Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond B 270: 2485-2489.
46. Sandell MI, Tobler M, Hasselquist D (2009) Yolk androgens and the development of avian immunity: an experiment in jackdaws (Corvus monedula). J Exp Biol 212: 815-822.
47. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90: 11446-11450.
48. Schwabl H (1996) Maternal testosterone in avian eggs enhances postnatal growth. Comp Biochem Physiol 114: 271-276.
49. Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15: 397-402.
50. Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267: 1451-1456.
51. Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham.
52. Tobler M, Sandell MI (2009) Sex-specific effects of prenatal testosterone on nestling plasma antioxidant capacity in the zebra finch. J Exp Biol 212: 89-94.
53. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary sex ratio of offspring. Science 179: 90-92.
54. Verboven N, Monaghan P, Evans DM et al (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.
55. von Engelhardt N, Carere C, Dijkstra C, Groothuis TGG (2006) Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc Lond B 273: 65-70.
56. von Schantz T, Bensch S, Grahn M et al (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266: 1-12.
57. Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton.
58. Williamson KA, Surai PF, Graves JA (2006) Yolk antioxidants and mate attractiveness in the Zebra Finch. Funct Ecol 20: 354-359.