Hormone levels predict individual differences in reproductive success in a passerine bird

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1717, 2011, Pages 2537-2545

  Ouyang, Jenny Q ^a   Sharp, Peter J ^b   Dawson, Alistair ^c   Quetting, Michael ^d   Hau, Michaela ^d  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^d MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

Corticosterone; Parental investment; Passer domesticus; Prolactin; Stress

Indexed keywords

CORTICOSTERONE; PROLACTIN;

BREEDING SEASON; BROOD REARING; CONCENTRATION (COMPOSITION); ENVIRONMENTAL STRESS; FITNESS; HORMONE; INDIVIDUAL VARIATION; LIFE HISTORY TRAIT; NATURAL SELECTION; PARENTAL INVESTMENT; PASSERINE; PHENOTYPIC PLASTICITY; REPRODUCTIVE SUCCESS; SEASONAL VARIATION;

ANIMAL; ARTICLE; BLOOD; FEMALE; MALE; MATERNAL BEHAVIOR; NESTING; PATERNAL BEHAVIOR; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REPRODUCTION; SEASON; SEX DIFFERENCE; SPARROW; UNITED STATES;

ANIMALS; CORTICOSTERONE; FEMALE; MALE; MATERNAL BEHAVIOR; NESTING BEHAVIOR; NEW JERSEY; PATERNAL BEHAVIOR; PROLACTIN; REPRODUCTION; SEASONS; SEX FACTORS; SPARROWS; STRESS, PHYSIOLOGICAL;

AVES; PASSER DOMESTICUS; PASSERIFORMES;

EID: 79960142332     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.2490     Document Type: Article

References (71)

1. Adkins-Regan, E. 2005 Hormones and animal social behavior.Princeton, NJ: Princeton University Press.
2. Ketterson, E. D. & Nolan, V. J. 1992 Hormones and lifehistories: an integrative approach. Am. Nat. 140, S33-S62.(doi:10.1086/285396)
3. Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D., Lynn, S., Ramenofsky, M. & Richardson, R. D.1998 Ecological bases of hormone-behavior interactions:the 'emergency life history stage'. Am. Zool. 38, 191-206.
4. Zera, A. J., Harshman, L. G. & Williams, T. D. 2007Evolutionary endocrinology: the developing synthesisbetween endocrinology and evolutionary genetics. Ann.Rev. Ecol. Evol. Syst. 38, 793-817. (doi:10.1146/annurev.ecolsys.38.091206.095615)
5. Bonier, F., Martin, P. R., Moore, I. T. & Wingfield, J. C.2009 Do baseline glucocorticoids predict fitness? TrendsEcol. Evol. 24, 634-642. (doi:10.1016/j.tree.2009.04.013)
6. Sinervo, B. & Licht, P. 1991 Hormonal and physiologicalcontrol of clutch size, egg size, and egg shape in sideblotchedlizards (Uta stansburiana)-constraints on theevolution of lizard life histories. J. Exper. Zool. 257,252-264. (doi:10.1002/jez.1402570216)
7. Williams, T. D. 2008 Individual variation in endocrinesystems: moving beyond the 'tyranny of the goldenmean'. Phil. Trans. R. Soc. B 363, 1687-1698. (doi:10.1098/rstb.2007.0003)
8. Bennett, A. F. 1987 Interindividual variability: an underutilizedresource. In New directions in ecological physiology(eds M. E. Feder, A. F. Bennett, W. W. Burggren &R. B. Huey), pp. 147-169. Cambridge, UK: CambridgeUniversity Press.
9. Kempenaers, B., Peters, A. & Foerster, K. 2008 Sourcesof individual variation in plasma testosterone levels. Phil.Trans. R. Soc. B 363, 1711-1723. (doi:10.1098/rstb.2007.0001)
10. Dingemanse, N. J., Edelaar, P. & Kempenaers, B. 2010Why is there variation in baseline glucocorticoid levels?Trends Ecol. Evol. 25, 261-262. (doi:10.1016/j.tree.2010.01.008)
11. McGlothlin, J. W., Whittaker, D. J., Schrock, S. E., Gerlach, N. M., Jawor, J. M., Snajdr, E. A. & Ketterson, E. D. 2010 Natural selection on testosterone productionin a wild songbird population. Am. Nat. 175, 687-701.(doi:10.1086/652469)
12. Zera, A. J. & Harshman, L. G. 2001 The physiology oflife history trade-offs in animals. Ann. Rev. Ecol. Syst. 32,95. (doi:10.1146/annurev.ecolsys.32.081501.114006)
13. Reed, W. L., Clark, M. E., Parker, P. G., Raouf, S. A., Arguedas, N., Monk, D. S., Snajdr, E., Nolan, V. & Ketterson, E. D. 2006 Physiological effects on demography:a long-term experimental study of testosterone'seffects on fitness. Am. Nat. 167, 667-683. (doi:10.1086/503054)
14. Sinervo, B., Miles, D.B., Frankino, W.A., Klukowski, M. & DeNardo, D. F. 2000 Testosterone, endurance, and Darwinianfitness: natural and sexual selection on thephysiological bases of alternative male behaviors in sideblotchedlizards. Horm. Behav. 38, 222-233. (doi:10.1006/hbeh.2000.1622)
15. Trainor, B. C. & Marler, C. A. 2001 Testosterone,paternal behavior, and aggression in the monogamousCalifornia mouse, Peromyscus californicus. Horm. Behav.40, 32-42. (doi:10.1006/hbeh.2001.1652)
16. Badyaev, A. V. & Duckworth, R. A. 2005 Evolution ofplasticity in hormonally-integrated parental tactics. InFunctional avian endocrinology (eds A. Dawson & P. J.Sharp), pp. 375-386. New Delhi, India: Narosa PublishingHouse.
17. Chastel, O., Lacroix, A., Weimerskirch, H. & Gabrielsen, G. W. 2005 Modulation of prolactin but not corticosteroneresponses to stress in relation to parental effort in along-lived bird. Horm. Behav. 47, 459-466. (doi:10.1016/j.yhbeh.2004.10.009)
18. Schradin, C. 2008 Differences in prolactin levels betweenthree alternative male reproductive tactics in striped mice(Rhabdomys pumilio). Proc. R. Soc. B 275, 1047-1052.(doi:10.1098/rspb.2008.0004)
19. Angelier, F. & Chastel, O. 2009 Stress, prolactin andparental investment in birds: a review. Gen. Comp. Endocrinol.163, 142-148. (doi:10.1016/j.ygcen.2009.03.028)
20. Angelier, F., Wingfield, J. C., Weimerskirch, H. & Chastel, O. 2010 Hormonal correlates of individual qualityin a long-lived bird: a test of the 'corticosterone-fitness hypothesis'. Biol. Lett. 6, 846-849. (doi:10.1098/rsbl.2010.0376)
21. Bonier, F., Martin, P. R., Sheldon, K. S., Jensen, J. P.,Foltz, S. L. & Wingfield, J. C. 2007 Sex-specific consequencesof life in the city. Behav. Ecol. 18, 121-129.(doi:10.1093/beheco/arl050)
22. Schoech, S. J., Rensel, M. A., Bridge, E. S., Boughton, R. K. & Wilcoxen, T. E. 2009 Environment, glucocorticoids,and the timing of reproduction. Gen. Comp.Endocrinol. 163, 201-207. (doi:10.1016/j.ygcen.2008.09.009)
23. Foerster, S. & Monfort, S. L. 2010 Fecal glucocorticoidsas indicators of metabolic stress in female Sykes' monkeys(Cercopithecus mitis albogularis). Horm. Behav. 58, 685-697.(doi:10.1016/j.yhbeh.2010.06.002)
24. Lendvai, A. Z., Giraudeau, M. & Chastel, O. 2007Reproduction and modulation of the stress response: anexperimental test in the house sparrow. Proc. R. Soc. B274, 391-397. (doi:10.1098/rspb.2006.3735)
25. Love, O. P., Breuner, C. W., Vezina, F. & Williams, T. D.2004 Mediation of a corticosterone-induced reproductiveconflict. Horm. Behav. 46, 59-65. (doi:10.1016/j.yhbeh.2004.02.001)
26. Angelier, F., Clement-Chastel, C.,Welcker, J., Gabrielsen,G.W. & Chastel, O. 2009 How does corticosterone affectparental behaviour and reproductive success? A study ofprolactin in black-legged kittiwakes. Funct. Ecol. 23,784-793. (doi:10.1111/j.1365-2435.2009.01545.x)
27. Silverin, B., Arvidsson, B. & Wingfield, J. 1997 Theadrenocortical responses to stress in breeding WillowWarblers Phylloscopus trochilus in Sweden: effects of latitudeand gender. Funct. Ecol. 11, 376-384. (doi:10.1046/j.1365-2435.1997.00097.x)
28. Horak, P., Mand, R. & Ots, I. 1997 Identifying targets ofselection: a multivariate analysis of reproductive traits inthe Great Tit. Oikos 78, 592-600. (doi:10.2307/3545622)
29. Cresswell, W. & McCleery, R. 2003 How Great Tits maintainsynchronization of their hatch date with food supplyin response to long-term variability in temperature.J. Anim. Ecol. 72, 356-366. (doi:10.1046/j.1365-2656.2003.00701.x)
30. Meijer, T., Daan, S. & Hall, M. 1990 Family planning inthe kestrel (Falco tinnunculus): the proximate control ofcovariation of laying date and clutch size. Behav. 114,117-136. (doi:10.1163/156853990X00077)
31. Vitousek, M. N., Mitchell, M. A., Romero, L. M., Awerman, J. & Wikelski, M. 2010 To breed or not tobreed: physiological correlates of reproductive status ina facultatively biennial iguanid. Horm. Behav. 57, 140-146. (doi:10.1016/j.yhbeh.2009.09.020)
32. Goutte, A., Antoine, É., Weimerskirch, H. & Chastel, O.2010 Age and the timing of breeding in a long-lived bird:a role for stress hormones? Funct. Ecol. 24, 1007-1016.(doi:10.1111/j.1365-2435.2010.01712.x)
33. Lancaster, L. T., Hazard, L. C., Clobert, J. & Sinervo, B. R. 2008 Corticosterone manipulation reveals differencesin hierarchical organization of multidimensionalreproductive trade-offs in r-strategist and K-strategistfemales. J. Evol. Biol. 21, 556-565. (doi:10.1111/j.1420-9101.2007.01478.x)
34. Ringsby, T. H., Berge, T., Saether, B. E. & Jensen, H.2009 Reproductive success and individual variation infeeding frequency of House Sparrows (Passer domesticus).J. Ornithol. 150, 469-481. (doi:10.1007/s10336-008-0365-z)
35. Buntin, J. D. 1996 Neural and hormonal control of parentalbehavior in birds. In Parental care: evolution,mechanisms, and adaptive significance, vol. 25 (eds J. S.Rosenblatt & C. T. Snowdon), pp. 161-213. Advancesin the Study of Behavior. New York, NY: AcademicPress Ltd.
36. Sharp, P. J., Dawson, A. & Lea, R. E. 1998 Control ofluteinizing hormone and prolactin secretion in birds. Comp. Biochem. Physiol. C 119, 275-282. (doi:10.1016/S0742-8413(98)00016-4)
37. Dawson, A. & Goldsmith, A. R. 1985 Modulation ofgonadotrophin and prolactin secretion by daylength andbreeding behaviour in free-living starlings Sturnusvulgaris. J. Zool. Lond. A 206, 241-252. (doi:10.1111/j.1469-7998.1985.tb05648.x)
38. Sockman, K. W., Sharp, P. J. & Schwabl, H. 2006Orchestration of avian reproductive effort: an integrationof the ultimate and proximate bases for flexibility inclutch size, incubation behaviour, and yolk androgendeposition. Biol. Rev. 81, 629-666. (doi:10.1017/S1464793106007147)
39. Bonier, F., Moore, I. T., Martin, P. R. & Robertson, R. J.2009 The relationship between fitness and baselineglucocorticoids in a passerine bird. Gen. Comp. Endocrinol.163, 208-213. (doi:10.1016/j.ygcen.2008.12.013)
40. Sapolsky, R. M., Romero, L. M. & Munck, A. U. 2000How do glucocorticoids influence stress responses?Integrating permissive, suppressive, stimulatory, and preparativeactions. Endocr. Rev. 21, 55-89. (doi:10.1210/er.21.1.55)
41. Wingfield, J. C. & Romero, L. M. 2001 Adrenocorticalresponses to stress and their modulation in free-livingvertebrates. In Handbook of physiology; section 7: theendocrine system; volume IV: coping with the environment:neural and endocrine mechanisms (eds B. S. McEwen &H. M. Goodman), pp. 211-234. New York, NY:Oxford University Press.
42. Wingfield, J. C. & Sapolsky, R. M. 2003 Reproduction andresistance to stress: when and how. J. Neuroendocrinol. 15,711-724. (doi:10.1046/j.1365-2826.2003.01033.x)
43. Altmann, J. 1974 Observational study of behaviour:sampling methods. Behaviour 49, 227-267. (doi:10.1163/156853974X00534)
44. Summers-Smith, J. D. 1963 The house sparrow. London,UK: Collins.
45. Breuner, C. W. & Orchinik, M. 2001 Seasonal regulationof membrane and intracellular corticosteroid receptors inthe house sparrow brain. J. Neuroendocrinol. 13, 412-420.(doi:10.1046/j.1365-2826.2001.00646.x)
46. Gill, S. A., Costa, L. M. & Hau, M. 2008 Males of asingle-brooded tropical bird species do not showincreases in testosterone during social challenges. Horm.Behav. 54, 115-124. (doi:10.1016/j.yhbeh.2008.02.003)
47. Bentley, G. E., Goldsmith, A. R., Dawson, A., Glennie, L. M., Talbot, R. T. & Sharp, P. J. 1997 Photorefractorinessin European starlings (Sturnus vulgaris) is notdependent upon the long-day-induced rise in plasmathyroxine. Gen. Comp. Endocrinol. 107, 428-438.(doi:10.1006/gcen.1997.6941)
48. Lessells, C. M. & Boag, P. T. 1987 Unrepeatable repeatabilities:a common mistake. Auk 104, 116-121.
49. Gienapp, P. & Visser, M. E. 2006 Possible fitness consequencesof experimentally advanced laying dates in GreatTits: differences between populations in different habitats. Funct. Ecol. 20, 180-185. (doi:10.1111/j.1365-2435.2006.01079.x)
50. Hegner, R. E. & Wingfield, J. C. 1987 Effects of brood-sizemanipulations on parental investment, breeding success,and reproductive endocrinology of house sparrows. Auk104, 470-480. (doi:10.1111/j.1420-9101.2005.01034.x)
51. Sharp, P. J. & Sreekumar, K. P. 2001 Photoperiodiccontrol of prolactin secretion. In Avian endocrinology(eds A. Dawson & C. M. Chaturved), pp. 245-255.New Delhi, India: Narosa Publishing House.
52. Breitenbach, R. P., Nagra, C. L. & Meyer, R. K. 1965Studies of incubation and broody behaviour in the pheasant(Phasianus colchicus). Anim. Behav. 13, 143-148.(doi:10.1016/0003-3472(65)90084-9)
53. Sockman, K. W., Schwabl, H. & Sharp, P. J. 2000 Therole of prolactin in the regulation of clutch size andonset of incubation behavior in the American Kestrel. Horm. Behav. 38, 168-176. (doi:10.1006/hbeh.2000.1616)
54. O'Dwyer, T. W., Buttemer, W. A., Priddel, D. M. & Downing, J. A. 2006 Prolactin, body condition and thecost of good parenting: an interyear study in a longlivedseabird, Gould's Petrel (Pterodroma leucoptera). Funct. Ecol. 20, 806-811. (doi:10.1111/j.1365-2435.2006.01168.x)
55. Wilson, A. J. & Nussey, D. H. 2009 What is individualquality? An evolutionary perspective. Trends Ecol. Evol.25, 207-214. (doi:10.1016/j.tree.2009.10.002)
56. Landys, M. M., Ramenofsky, M. & Wingfield, J. C. 2006Actions of glucocorticoids at a seasonal baseline as comparedto stress-related levels in the regulation of periodiclife processes. Gen. Comp. Endocrinol. 148, 132-149.(doi:10.1016/j.ygcen.2006.02.013)
57. Romero, L. M. 2002 Seasonal changes in plasma glucocorticoidconcentrations in free-living vertebrates. Gen.Comp. Endocrinol. 128, 1-24. (doi:10.1016/S0016-6480(02)00064-3)
58. Hau, M., Ricklefs, R. E., Wikelski, M., Lee, K. A. & Brawn, J. D. 2010 Cortiocosterone, testosterone, andlife-history strategies of birds. Proc. R. Soc. B 277, 3203-3212. (doi:10.1098/rspb.2010.0673)
59. Romero, L. M. 2004 Physiological stress in ecology:lessons from biomedical research. Trends Ecol. Evol.19, 249-255. (doi:10.1016/j.tree.2004.03.008)
60. Dawson, A. & Goldsmith, A. R. 1982 Prolactin and gonadotrophinsecretion in wild starlings (Sturnus vulgaris)during the annual cycle and in relation to nesting, incubation,and rearing young. Gen. Comp. Endocrinol. 48,213-221. (doi:10.1016/0016-6480(82)90019-3)
61. Wingfield, J. C. & Goldsmith, A. R. 1990 Plasma levelsof prolactin and gonadal steroids in relation to multiplebroodingand renesting in free-living populations of thesong sparrow Melospiza melodia. Horm. Behav. 24,89-103. (doi:10.1016/0018-506X(90)90029-W)
62. Moore, I. T., Bonier, F. & Wingfield, J. C. 2005 Reproductiveasynchrony and population divergence betweentwo tropical bird populations. Behav. Ecol. 16,755-762. (doi:10.1093/beheco/ari049)
63. Silverin, B. 1986 Corticosterone-binding proteins andbehavioral effects of high plasma levels of corticosteroneduring the breeding period in the pied flycatcher. Gen.Comp. Endocrinol. 64, 67-74. (doi:10.1016/0016-6480(86)90029-8)
64. Wingfield, J. C., Oreilly, K. M. & Astheimer, L. B. 1995Modulation of the adrenocortical responses to acutestress in arctic birds-a possible ecological basis. Am.Zool. 35, 285-294. (doi:10.1093/icb/35.3.285)
65. Romero, L. M., Dickens, M. J. & Cyr, N. E. 2009 Thereactive scope model-a new model integrating homeostasis,allostasis, and stress. Horm. Behav. 55, 375-389.(doi:10.1016/j.yhbeh.2008.12.009)
66. McGlothlin, J. W. & Ketterson, E. D. 2008 Hormonemediatedsuites as adaptations and evolutionary constraints. Phil. Trans. R. Soc. B 363, 1611-1620.(doi:10.1098/rstb.2007.0002)
67. Evans, M. R., Roberts, M. L., Buchanan, K. L. &Goldsmith A. R. 2006 Heritability of corticosteroneresponse and changes in life history traits during selectionin the zebra finch journal>J. Evol. Biol. 19, 343-352. (doi:10.1111/j.1420-9101.2005.01034.x)
68. Satterlee, D. G. & Johnson, W. A. 1988 Selection ofJapanese quail for contrasting blood corticosteroneresponse to immobilization. Poultry Sci. 67, 25-32.
69. Nussey, D. H., Wilson, A. J. & Brommer, J. E. 2007 Theevolutionary ecology of individual phenotypic plasticity inwild populations. J. Evol. Biol. 20, 831-844. (doi:10.1111/j.1420-9101.2007.01300.x)
70. Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M. & Lessells, C. M. 1998 Warmer springs lead to mistimedreproduction in Great Tits (Parus major). Proc. R. Soc.Lond. B 265, 1867-1870. (doi:10.1098/rspb.1998.0514)
71. Whitekiller, R. R., Westneat, D. F., Schwagmeyer, P. L. & Mock, D. W. 2000 Badge size and extra-pair fertilizationsin the House Sparrow. Condor 102, 342-348. (doi:10.1650/0010-5422(2000)102[0342:BSAEPF]2.0.CO;2)