Brood Reduction via Intra-clutch Variation in Testosterone - An Experimental Test in the Great Tit

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Podlas, Katarzyna ^a   Helfenstein, Fabrice ^a,b   Richner, Heinz ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

SESAME SEED OIL; TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; BREEDING METHOD; BROOD REDUCTION; CHICK; CONTROLLED STUDY; EGG; EGG LAYING; EGG YOLK; EXPERIMENTAL TEST; FEMALE; HATCHING; INTRA CLUTCH VARIATION; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIATION; POULTRY FARMING; PROGENY; SIBLING;

ANIMALS; BIRDS; EGG YOLK; FEMALE; OVIPOSITION; REPRODUCTION; TESTOSTERONE;

EID: 84874248030     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056672     Document Type: Article

References (90)

1. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. New York: Oxford University Press. 400 p.
2. Biere A, (1991) Parental effects in lychnis-flos-cuculi. 1. Seed size, germination and seedling performance in a controlled environment. J Evol Biol 4: 447-465.
3. Montalvo AM, Shaw RG, (1994) Quantitative genetics of sequential life-history and juvenile traits in the partially selfing perennial (Aquilegia-caerulea). Evolution 48: 828-841.
4. Schwaegerle KE, Levin DA, (1990) Environmental effects on growth and fruit production in phlox-drummondii. J Ecol 78: 15-26.
5. Bernardo J, (1996) Maternal effects in animal ecology. Am Zool 36: 83-105.
6. Parichy DM, Kaplan RH, (1992) Maternal effects on offspring growth and development depend on environmental quality in the frog Bombina-orientalis. Oecologia 91: 579-586.
7. Groothuis TGG, Eising CM, Dijkstra C, Muller W, (2005) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett 1: 78-81.
8. Ford JJ, (1982) Testicular control of defeminization in male pigs. Biol Reprod 27: 425-430.
9. Groothuis TGG, Schwabl H, (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc B-Biol Sci 363: 1647-1661.
10. Janzen FJ, Wilson ME, Tucker JK, Ford SP, (1998) Endogenous yolk steroid hormones in turtles with different sex-determining mechanisms. Gen Comp Endocrinol 111: 306-317.
11. Nelson RJ (2000) An introduction to behavioral endocrinology. New York: Sunderland. 712 p.
12. Clark MM, Galef BG, (1995) A gerbil dams fetal intrauterine position affects the sex-ratios of litters she gestates. Physiol Behav 57: 297-299.
13. Grant VJ, (1994) Maternal dominance and the conception of sons. Br J Med Psychol 67: 343-351.
14. Schwabl H, (1993) Yolks is a source of maternal testosterone for developing birds. P Natl Acad Sci USA 90: 11446-11450.
15. Bate LA, Kreukniet MB, Hacker RR, (1985) The relationship between serum testosterone levels, sex and teat-seeking ability of newborn piglets. Can J Anim Sci 65: 627-630.
16. Dloniak SM, French JA, Holekamp KE, (2006) Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas. Nature 440: 1190-1193.
17. Manikkam M, Crespi EJ, Doop DD, Herkimer C, Lee JS, et al. (2004) Fetal programming: Prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 145: 790-798.
18. McCormick MI, (1999) Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 118: 412-422.
19. Clark MM, Moghaddas M, Galef BG, (2002) Age at first mating affects parental effort and fecundity of female mongolian gerbils. Anim Behav 63: 1129-1134.
20. Eising CM, Muller W, Groothuis TGG, (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2: 20-22.
21. Gil D, (2008) Hormones in avian eggs: Physiology, ecology and behavior. In: Advances in the Study of Behavior, Vol Brockmann HJ, Roper TJ, Naguib M, Wynne-Edwards KE, Barnard C, et al., editors. editors. 38: 337-398.
22. Smith AS, French JA, (2008) Maternal androgen levels during pregnancy are associated with early-life growth and aggressive behavior of offspring in geoffroys marmosets (Callithrix geoffroyi). Am J Primatol 70: 46-46.
23. Strasser R, Schwabl H, (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56: 491-497.
24. Oyegbile TO, Marler CA, (2005) Winning fights elevates testosterone levels in california mice and enhances future ability to win fights. Horm Behav 48: 259-267.
25. vom Saal FS, (1989) Sexual differentiation in litter-bearing mammals: influence of sex of adjacent fetuses in utero. Journal of animal science 67: 1824-1840.
26. Dvorak M, (1981) Influence of neonatal application of testosterone on the growth piglets. Vet Med Czech 26: 65-73.
27. Navara KJ, Hill GE, Mendonca MT, (2006) Yolk androgen deposition as a compensatory strategy. Behav Ecol Sociobiol 60: 392-398.
28. Schwabl H, (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comparative Biochemistry and Physiology 114: 271-276.
29. Kaiser S, Sachser N, (2005) The effects of prenatal social stress on behaviour: mechanisms and function. Neuroscience & Biobehavioral Reviews 29: 283-294.
30. Albert DJ, Jonik RH, Walsh ML, Petrovic DM, (1989) Testosterone supports hormone-dependent aggression in female rats. Physiol Behav 46: 185-189.
31. Eising CM, Groothuis TGG, (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66: 1027-1034.
32. Nelson RJ (2006) Biology of agression. New York: Oxford University Press. 528 p.
33. Hudson R, Trillmich F, (2008) Sibling competition and cooperation in mammals: challenges, developments and prospects. Behav Ecol Sociobiol 62: 299-307.
34. Urban RJ, (2011) Growth, hormone and testosterone: anabolic effects on muscle. Hormone Research in Paediatrics 76: 81-83.
35. 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.
36. Randall P, (2002) The "levator septi nasi muscle" and its clinical significance- Discussion. Plast Reconstr Surg 109: 1713-1713.
37. Staub NL, DeBeer M, (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108: 1-24.
38. Andersson S, Uller T, Lohmus M, Sundstrom F, (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol 17: 501-505.
39. Muller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, et al. (2005) Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc R Soc B 272: 1971-1977.
40. Wolf CJ, Hotchkiss A, Ostby JS, LeBlanc GA, Gray LE, (2002) Effects of prenatal testosterone propionate on the sexual development of male and female rats: a dose-response study. Toxicol Sci 65: 71-86.
41. Alexander J, Stimson WH, (1988) Sex-hormones and the course of parasitic infection. Parasitol Today 4: 189-193.
42. Gaillard RC, Spinedi E, (1998) Sex- and stress-steroids interactions and the immune system: evidence for a neuroendocrine-immunological sexual dimorphism. Domest Anim Endocrin 15: 345-352.
43. Grossman CJ, (1985) Interactions between the gonadal-steroids and the immune system. Science 227: 257-261.
44. Martin JT, (2000) Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur J Pharmacol 405: 251-261.
45. Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H, (2005) Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol 74: 675-682.
46. Rosser CB, Herkimer C, Sarma HN, Recabarren SE, Dunaif A, et al. (2003) Fetal programming: Prenatal exposure to excess testosterone programs hyperinsulinemia. Biol Reprod 68: 293-293.
47. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G, (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc B 274: 819-825.
48. Fisher MO, Nager RG, Monaghan P, (2006) Compensatory growth impairs adult cognitive performance. Plos Biol 4: 1462-1466.
49. Hales CN, Desai M, Ozanne SE, Crowther NJ, (1996) Fishing in the stream of diabetes: From measuring insulin to the control of fetal organogenesis. Biochem Soc Trans 24: 341-350.
50. Okuliarova M, Kostal L, Zeman M, (2011) Effects of divergent selection for yolk testosterone content on growth characteristics of japanese quail. Comp Biochem Physiol A-Mol Integr Physiol 160: 81-86.
51. Verboven N, Monaghan P, Evans DM, Schwabl H, Evans N, 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.
52. Lovern MB, Wade J, (2001) Maternal plasma and egg yolk testosterone concentrations during embryonic development in green anoles (Anolis carolinensis). Gen Comp Endocrinol 124: 226-235.
53. Slob AK, Ooms MP, Vreeburg JTM, (1980) Prenatal and early postnatal sex-differences in plasma and gonadal testosterone and plasma luteinizing-hormone in female and male rats. J Endocrinol 87: 81-87.
54. Lipar JL, Ketterson ED, Nolan V, (1999) Intraclutch variation in testosterone content of red-winged blackbird eggs. Auk 116: 231-235.
55. Gil D, Graves J, Hazon N, Wells A, (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286: 126-128.
56. Schwabl H, Mock DW, Gieg JA, (1997) A hormonal mechanism for parental favouritism. Nature 386: 231-231.
57. Schwabl H (1997) Control of offspring fitness by maternal hormones; Kawashima S, Kikuyama S, editors. 40128 Bologna: Medimond S R L. 1677-1682 p.
58. Royle NJ, Surai PF, Hartley IR, (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12: 381-385.
59. Beissinger SR, Stoleson SH, (1997) Hatching asynchrony in birds. Trends Ecol Evol 12: 112-112.
60. Mock DW, Parker GA (1997) The evolution of sibling rivalry. New York: Oxford University Press. 480 p.
61. Schwabl H, (1996) Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool 276: 157-163.
62. Eising CM, Eikenaar C, Schwbl H, Groothuis TGG, (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268: 839-846.
63. Groothuis TGG, Carere C, Lipar J, Drent PJ, Schwabl H, (2008) Selection on personality in a songbird affects maternal hormone levels tuned to its effect on timing of reproduction. Biol Lett 4: 465-467.
64. Muller 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.
65. Sockman KW, Schwabl H, (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267: 1451-1456.
66. 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.
67. Tschirren B, Richner H, Schwabl H, (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc Lond B 271: 1371-1375.
68. Pettifor RA, Perrins CM, McCleery RH, (2001) The individual optimization of fitness: variation in reproductive output, including clutch size, mean nestling mass and offspring recruitment, in manipulated broods of great tits (Parus major). J Anim Ecol 70: 62-79.
69. Amundsen T, Slagsvold T, (1998) Hatching asynchrony in great tits: A bet-hedging strategy? Ecology 79: 295-304.
70. Remeš V, (2011) Yolk androgens in great tit eggs are related to male attractiveness, breeding density and territory quality. Behav Ecol Sociobiol 65: 1257-1266.
71. Bruggeman V, Van As P, Decuypere E, (2002) Developmental endocrinology of the reproductive axis in the chicken embryo. Comparative Biochemistry and Physiology- Part a: Molecular and Integrative Physiology 131: 839-846.
72. Palme R, Möstl E, (1994) Biotin-streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar faeces. In: Advances in Steroid Analysis 1993: Proceedings of the 5th Symposium on the Analysis of Steroids Held at Szombathely, Hungary, May 3-5, 1993: Akadémiai Kiadó Görög S, editor. 1994: 111-117.
73. Mostl E, Spendier H, Kotrschal K, (2001) Concentration of immunoreactive progesterone and androgens in the yolk of hens' eggs (Gallus domesticus). Wiener Tierarztliche Monatsschrift 88: 62-65.
74. R Development Core Team (2007) R: A language and environmental for statistical computing. Vienna: R Foundation for statistical computing.
75. van de Pol M, Wright J, (2009) A simple method for distinguishing within- versus between-subject effects using mixed models. Anim Behav 77: 753-758.
76. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. New York: Springer. 530 p.
77. Hadfield J (2012) MCMCglmm Course Notes.
78. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. New York: Springer. 574 p.
79. Dijkstra C, Daan S, Pen I, (1998) Fledgling sex ratios in relation to brood size in size-dimorphic altricial birds. Behav Ecol 9: 287-296.
80. Neuenschwander S, Brinkhof MWG, Kölliker M, Richner H, (2003) Brood size, sibling competition, and the cost of begging in great tits (Parus major). Behav Ecol 14: 457-462.
81. Galvan I, Alonso-Alvarez C, (2010) Yolk testosterone shapes the expression of a melanin-based signal in great tits: an antioxidant-mediated mechanism? J Exp Biol 213: 3127-3130.
82. Pitala N, Ruuskanen S, Laaksonen T, Doligez B, Tschirren B, et al. (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.
83. Ruuskanen S, Laaksonen T, (2010) Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca). Horm Behav 57: 119-127.
84. Fennell MJ, Scanes CG, (1992) Inhibition of growth in chickens by testosterone, 5-alpha dihydrotestosterone and 19-nortestosterone. Poultry Science 71: 357-366.
85. Ros AFH, (1999) Effects of testosterone on growth, plumage pigmentation, and mortality in black-headed gull chicks. Ibis 141: 451-459.
86. Tobler M, Nilsson JA, Nilsson JF, (2007) Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol Lett 3: 408-410.
87. Berthouly A, Helfenstein F, Richner H, (2007) Cellular immune response, stress resistance and competitiveness in nestling great tits in relation to maternally transmitted carotenoids. Funct Ecol 21: 335-343.
88. Saino N, Dall'Ara P, Martinelli R, Moller AP, (2002) Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow. J Evol Biol 15: 735-743.
89. Morales J, Sanz JJ, Moreno J, (2006) Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biol Lett 2: 334-336.
90. Carere C, Balthazart J, (2007) Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends in Endocrinology & Metabolism 18: 73-80.