Penguin chicks benefit from elevated yolk androgen levels under sibling competition

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Poisbleau, Maud ^a   Müller, Wendt ^a   Carslake, David ^b   Demongin, Laurent ^a   Groothuis, Ton G G ^c   van Camp, Jeff ^a   Eens, Marcel ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROSTANOLONE; ANDROSTENEDIONE; TESTOSTERONE;

ANDROGEN THERAPY; ARTICLE; CHICK; CONTROLLED STUDY; EGG; EGG LAYING; EGG YOLK; EMBRYO DEVELOPMENT; EUDYPTES; EUDYPTES CHRYSOCOME; FEMALE; GROWTH; HATCHING; INTRASPECIFIC COMPETITION; MALE; NESTING; NONHUMAN; PENGUIN; SIBLING COMPETITION;

ANDROGENS; ANIMALS; EMBRYONIC DEVELOPMENT; SPHENISCIDAE; YOLK SAC;

EUDYPTES; EUDYPTES CHRYSOCOME; SPHENISCIDAE;

EID: 84864477802     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042174     Document Type: Article

References (58)

1. Lack D (1954) The natural regulation of animal numbers. Oxford: Clarendon.
2. Mock DW, Parker GA, (1998) Siblicide, family conflict and the evolutionary limits of selfishness. Animal Behaviour 56: 1-10.
3. Mock DW, Parker GA(1997) The evolution of sibling rivalry. Oxford University Press.
4. Lack D, (1947) The significance of clutch-size. Ibis 89: 302-352.
5. Amundsen T, Slagsvold T, (1991) Hatching asynchrony: facilitating adaptive or maladaptive brood reduction? In: Acta XX Congressus Internationalis Ornithologici. Bell BD, Cossee RO, Flux JEC, Heather BD, et al., editors. Wellington, New Zealand. pp. 1707-1719.
6. Magrath RD, (1990) Hatching asynchrony in altricial birds. Biological Reviews 65: 587-622.
7. Howe HF, (1978) Initial investment, clutch size, and brood reduction in the common grackle (Quiscalus quiscula L.). Ecology 59: 1109-1122.
8. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C, (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews 29: 329-352.
9. Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, et al. (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proceedings of the Royal Society of London, Series B: Biological Sciences 269: 1729-1733.
10. Gil D, (2008) Hormones in avian eggs: physiology, ecology and behavior. Advances in the Study of Behavior 38: 337-398.
11. Groothuis TGG, Schwabl H, (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philosophical Transactions of the Royal Society of London, series B: Biological Sciences 363: 1647-1661.
12. Müller W, Boonen S, Groothuis TGG, Eens M, (2010) Maternal yolk testosterone in canary eggs: toward a better understanding of mechanisms and function. Behavioral Ecology 21: 493-500.
13. Eising CM, Eikenaar C, Schwabl H, Groothuis TGG, (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proceedings of the Royal Society of London, Series B: Biological Sciences 268: 839-846.
14. 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. American Naturalist 178: 64-74.
15. Schwabl H, Mock DW, Gieg JA, (1997) A hormonal mechanism for parental favouritism. Nature 386: 231.
16. Reed WL, Vleck CM, (2001) Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128: 164-171.
17. Gil D, Heim C, Bulmer E, Rocha M, Puerta M, et al. (2004) Negative effects of early developmental stress on yolk testosterone levels in a passerine bird. Journal of Experimental Biology 207: 2215-2220.
18. Gil D, Graves J, Hazon N, Wells A, (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286: 126-128.
19. 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. Hormones and Behavior 45: 64-70.
20. Tschirren B, Richner H, Schwabl H, (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proceedings of the Royal Society of London, Series B: Biological Sciences 271: 1371-1375.
21. Groothuis TG, Schwabl H, (2002) Determinants of within- and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Functional Ecology 16: 281-289.
22. Warham J, (1975) The crested penguins. In: The biology of penguins. Stonehouse B, editor. London, UK: The Macmillan Press. pp. 189-269.
23. Williams TD(1995) The penguins. Oxford, UK: Oxford University Press.
24. Demongin L, Poisbleau M, Raya Rey A, Schiavini A, Quillfeldt P, et al. (2010) Geographical variation in egg size dimorphism in rockhopper penguins. Polar Biology 33: 469-476.
25. St Clair CC, (1996) Multiple mechanisms of reversed hatching asynchrony in rockhopper penguins. Journal of Animal Ecology 65: 485-494.
26. St Clair CC, (1998) What is the function of first eggs in crested penguins? Auk 115: 478-482.
27. Poisbleau M, Demongin L, Strange IJ, Otley H, Quillfeldt P, (2008) Aspects of the breeding biology of the southern rockhopper penguin Eudyptes c. chrysocome and new consideration on the intrinsic capacity of the A-egg. Polar Biology 31: 925-932.
28. Lamey TC, (1990) Hatch asynchrony and brood reduction in penguins. In: Penguin biology. Davis LS, Darby JT, editors. San Diego: Academic Press. pp. 399-416.
29. von Engelhardt N, Groothuis TGG, (2011) Maternal hormones in avian eggs. In: Hormones and reproduction of vertebrates. Norris DO, Lopez KH, editors. Academic Press. pp. 91-127.
30. Poisbleau M, Demongin L, Chastel O, Eens M, Quillfeldt P, (2011) Yolk androgen deposition in rockhopper penguins, a species with reversed hatching asynchrony. General and Comparative Endocrinology 170: 622-628.
31. Poisbleau M, Carslake D, Demongin L, Eens M, Chastel O, et al. (2011) Yolk androgen deposition without an energetic cost for female rockhopper penguins: a compensatory strategy to accelerate brood reduction? Biology Letters 7: 605-607.
32. Moreno J, Barbosa A, Potti J, Merino S, (1997) The effects of hatching date and parental quality on chick growth and creching age in the chinstrap penguin (Pygoscelis antarctica): a field experiment. Auk 114: 47-54.
33. Eising CM, Groothuis TGG, (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Animal Behaviour 66: 1027-1034.
34. Poisbleau M, Demongin L, Angelier F, Dano S, Lacroix A, et al. (2009) What ecological factors can affect albumen corticosterone levels in the clutches of seabirds? Timing of breeding, disturbance and laying order in rockhopper penguins (Eudyptes chrysocome chrysocome). General and Comparative Endocrinology 162: 139-145.
35. Poisbleau M, Demongin L, Trouve C, Quillfeldt P, (2009) Maternal deposition of yolk corticosterone in clutches of southern rockhopper penguins (Eudyptes chrysocome chrysocome). Hormones and Behavior 55: 500-506.
36. Barnett CA, Clairardin SG, Thompson CF, Sakaluk SK, (2011) Turning a deaf ear: a test of the manipulating androgens hypothesis in house wrens. Animal Behaviour 81: 113-120.
37. Romano M, Rubolini D, Martinelli R, Alquati AB, Saino N, (2005) Experimental manipulation of yolk testosterone affects digit length ratios in the ring-necked pheasant (Phasianus colchicus). Hormones and Behavior 48: 342-346.
38. Bonisoli-Alquati A, Matteo A, Ambrosini R, Rubolini D, Romano M, et al. (2011) Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Hormones and Behavior 59: 75-82.
39. Poisbleau M, Demongin L, van Noordwijk HJ, Strange IJ, Quillfeldt P, (2010) Sexual dimorphism and use of morphological measurements to sex adults, immatures and chicks of rockhopper penguins. Ardea 98: 217-224.
40. Walsh PS, Metzger DA, Higuchi R, (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506-513.
41. Griffiths R, Double MC, Orr K, Dawson RJG, (1998) A DNA test to sex most birds. Molecular Ecology 7: 1701-1075.
42. Hinde CA, Buchanan KL, Kilner RM, (2009) Prenatal environmental effects match offspring begging to parental provisioning. Proceedings of the Royal Society of London, Series B: Biological Sciences 276: 2787-2794.
43. Müller W, Dijkstra C, Groothuis TGG, (2009) Maternal yolk androgens stimulate territorial behaviour in black-headed gull chicks. Biology Letters 5: 586-588.
44. von Engelhardt N, Carere C, Dijkstra C, Groothuis TGG, (2006) Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proceedings of the Royal Society of London, Series B: Biological Sciences 273: 65-70.
45. Müller W, Eens M, (2009) Elevated yolk androgen levels and the expression of multiple sexually selected male characters. Hormones and Behavior 55: 175-181.
46. Sockman KW, Schwabl H, (2000) Yolk androgens reduce offspring survival. Proceedings of the Royal Society of London, Series B: Biological Sciences 267: 1451-1456.
47. Boncoraglio G, Rubolini D, Romano M, Martinelli R, Saino N, (2006) Effects of elevated yolk androgens on perinatal begging behavior in yellow-legged gull (Larus michahellis) chicks. Hormones and Behavior 50: 442-447.
48. Andersson S, Uller T, Lõhmus M, Sundström F, (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. Journal of Evolutionary Biology 17: 501-505.
49. Rubolini D, Romano M, Martinelli R, Saino N, (2006) Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behavioral Ecology and Sociobiology 59: 344-352.
50. Massaro M, Davis LS, (2004) Preferential incubation positions for different sized eggs and their influence on incubation period and hatching asynchrony in Snares crested (Eudyptes robustus) and yellow-eyed penguins (Megadyptes antipodes). Behavioral Ecology and Sociobiology 56: 426-434.
51. Daisley JN, Bromundt V, Möstl E, Kotrschal K, (2005) Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japonese quail chicks Coturnix japonica. Hormones and Behavior 47: 185-194.
52. Navara KJ, Hill GE, Mendonça MT, (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiological and Biochemical Zoology 78: 570-578.
53. Mu X, LeBlanc GA, (2002) Developmental toxicity of testosterone in the crustacean Daphnia magna involves anti-ecdysteroidal activity. General and Comparative Endocrinology 129: 127-133.
54. Rutkowska J, Wilk T, Cichoń M, (2007) Androgen-dependent maternal effects on offspring fitness in zebra finches. Behavioral Ecology and Sociobiology 61: 1211-1217.
55. Sockman KW, Weiss J, Webster MS, Talbott V, Schwabl H, (2008) Sex-specific effects of yolk-androgens on growth of nestling American kestrels. Behavioral Ecology and Sociobiology 62: 617-625.
56. Ketterson ED, Nolan V Jr, (1992) Hormones and life histories: an integrative approach. American Naturalist 140: S33-S62.
57. Wingfield JC, Lynn SE, Soma KK, (2001) Avoiding the 'costs' of testosterone: ecological bases of hormone-behavior interactions. Brain, Behavior and Evolution 57: 239-251.
58. Müller W, Vergauwen J, Eens M, (2009) Long-lasting consequences of elevated yolk testosterone levels on female reproduction. Behavioral Ecology and Sociobiology 63: 809-816.