Developmental stress increases reproductive success in male zebra finches

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1795, 2014, Pages

  Crino, Ondi L ^a,b   Prather, Colin T ^b   Driscoll, Stephanie C ^b   Good, Jeffrey M ^b   Breuner, Creagh W ^b  

^a MACQUARIE UNIVERSITY   (Australia)

^b UNIVERSITY OF MONTANA   (United States)

Author keywords

Alternative reproductive tactic; Corticosterone; Developmental stress; Parental care; Reproductive success; Zebra finch

Indexed keywords

CORTICOSTERONE; PHARMACOLOGY;

ENVIRONMENTAL STRESS; EXTRA-PAIR COPULATION; HERITABILITY; LIFE HISTORY TRAIT; NESTLING; PARENTAL CARE; PASSERINE; PHENOTYPE; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; STEROID;

ANIMAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MALE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REPRODUCTION; SONGBIRD;

ANIMALS; CORTICOSTERONE; DRUG EFFECTS; GROWTH AND DEVELOPMENT; MALE; PHARMACOLOGY; PHYSIOLOGY; REPRODUCTION; SONGBIRDS; STRESS, PHYSIOLOGICAL;

TAENIOPYGIA GUTTATA;

EID: 84908125584     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1266     Document Type: Article

References (73)

1. Mousseau TA, Fox CW. 1998 The adaptive significance of maternal effects. Trends Ecol. Evol. 13, 403-407. (doi:10.1016/S0169-5347 (98)01472-4)
2. Sheldon BC. 2002 Adaptive maternal effects and rapid population differentiation. Trends Ecol. Evol. 17, 247-249. (doi:10.1016/S0169-5347(02) 02459-X)
3. Stamps J. 2003 Behavioural processes affecting development: Tinbergen's fourth question comes of age. Anim. Behav. 66, 1-13. (doi:10.1006/anbe. 2003.2180)
4. Henriksen R, Rettenbacher S, Groothuis TGG. 2011 Prenatal stress in birds: pathways, effects, function and perspectives. Neurosci. Biobehav. Rev. 35, 1484-1501. (doi:10.1016/j.neubiorev.2011.04.010)
5. Schoech SJ, Rensel MA, Heiss RS. 2011 Short- and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: a review. Curr. Zool. 57, 514-530.
6. Nesan D, Vijayan MM. 2013 Role of glucocorticoid in developmental programming: evidence from zebrafish. Gen. Comp. Endocrinol. 181, 35-44. (doi:10.1016/j.ygcen.2012.10.006)
7. Matthews SG. 2002 Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol. Metab. 13, 373-380. (doi:10.1016/ S1043-2760(02)00690-2)
8. Hayward LS, Wingfield JC. 2004 Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen. Comp. Endocrinol. 135, 365-371. (doi:10.1016/j. ygcen.2003.11.002)
9. Wada H, Salvante KG, Stables C, Wagner E, Williams TD, Breuner CW. 2008 Adrenocortical responses in zebra finches (Taeniopygia guttata): individual variation, repeatability, and relationship to phenotypic quality. Horm. Behav. 53, 472-480. (doi:10.1016/j.yhbeh.2007.11.018)
10. Tarlow EM, Wikelski M, Anderson DJ. 2001 Hormonal correlates of siblicide in Galapagos Nazca boobies. Horm. Behav. 40, 14-20. (doi:10.1006/ hbeh.2001.1661)
11. Kitaysky AS, Kitaiskaia EV, Wingfield JC, Piatt JF. 2001 Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J. Comp. Physiol. B 171, 701-709. (doi:10.1007/ s003600100230)
12. Blas J, Baos R, Bortolotti GR, Marchant T, Hiraldo F. 2005 A multi-tier approach to identifying environmental stress in altricial nestling birds. Funct. Ecol. 19, 315-322. (doi:10.1111/j.1365- 2435.2005.00976.x)
13. Spencer KA, Evans NP, Monaghan P. 2009 Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary- adrenal axis. Endocrinology 150, 1931-1934. (doi:10.1210/En.2008-1471)
14. Francis D, Diorio J, Liu D, Meaney MJ. 1999 Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155-1158. (doi:10.1126/science.286. 5442.1155)
15. Liu D et al. 1997 Maternal care, hippocampal glucocorticoid receptors, and hypothalamic- pituitary-adrenal responses to stress. Science 277, 1659-1662. (doi:10.1126/science.277.5332.1659)
16. Spencer KA, MacDougall-Shackleton SA. 2011 Singing to impress: the importance of developmental stress. Behav. Ecol. 22, 14-15. (doi:10.1093/beheco/arq116)
17. Monaghan P, Heidinger BJ, D'Alba L, Evans NP, Spencer KA. 2012 For better or worse: reduced adult lifespan following early-life stress is transmitted to breeding partners. Proc. R. Soc. B. 279, 709-714. (doi:10.1098/rspb.2011.1291)
18. Naguib M, Gil D. 2005 Transgenerational effects on body size caused by early developmental stress in zebra finches. Biol. Lett. 1, 95-97. (doi:10.1098/ rsbl.2004.0277)
19. Grindstaff JL, Hunsaker VR, Cox SN. 2012 Maternal and developmental immune challenges alter behavior and learning ability of offspring. Horm. Behav. 62, 337-344. (doi:10.1016/j.yhbeh. 2012.04.005)
20. Schmidt KL, MacDougall-Shackleton EA, MacDougall-Shackleton SA. 2012 Developmental stress has sex-specific effects on nestling growth and adult metabolic rates but no effect on adult body size or body composition in song sparrows. J. Exp. Biol. 215, 3207-3217. (doi:10.1242/Jeb. 068965)
21. Buchanan KL, Spencer KA, Goldsmith AR, Catchpole CK. 2003 Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc. R. Soc. B 270, 1149-1156. (doi:10.1098/rspb.2003.2330)
22. Nowicki S, Peters S, Podos J. 1998 Song learning, early nutrition and sexual selection in songbirds. Am. Zool. 38, 179-190. (doi:10.1093/icb/38.1.179)
23. Nowicki S, Searcy WA, Peters S. 2002 Brain development, song learning and mate choice in birds: a review and experimental test of the 'nutritional stress hypothesis'. J. Comp. Physiol. A 188, 1003-1014. (doi:10.1007/s00359-002-0361-3)
24. Roulin A, Almasi B, Rossi-Pedruzzi A, Ducrest AL, Wakamatsu K, Miksik I, Blount JD, Jenni-Eiermann S, Jenni L. 2008 Corticosterone mediates the condition-dependent component of melanin-based coloration. Anim. Behav. 75, 1351-1358. (doi:10. 1016/j.anbehav.2007.09.007)
25. Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK. 2003 Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm. Behav. 44, 132-139. (doi:10.1016/ S0018-506x(03)00124-7)
26. Wada H, Breuner CW. 2008 Transient elevation of corticosterone alters begging behavior and growth of white-crowned sparrow nestlings. J. Exp. Biol. 211, 1696-1703. (doi:10.1242/Jeb.009191)
27. Spencer KA, Wimpenny JH, Buchanan KL, Lovell PG, Goldsmith AR, Catchpole CK. 2005 Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata). Behav. Ecol. Sociobiol. 58, 423-428. (doi:10.1007/s00265-005-0927-5)
28. Hill GE. 1991 Plumage coloration is a sexually selected indicator of male quality. Nature 350, 337-339. (doi:10.1038/350337a0)
29. Taborsky M, Oliveira RF, Brockmann HJ. 2008 The evolution of alternative reproductive tactics: concepts and questions. In Alternative reproductive tactics: an integrative approach (eds RF Oliveira, M Taborsky, HJ Brockmann), pp. 1-21. New York, NY: Cambridge University Press.
30. Lank DB, Smith CM, Hanotte O, Burke T, Cooke F. 1995 Genetic polymorphism for alternative matingbehavior in lekking male ruff Philomachus pugnax. Nature 378, 59-62. (doi:10.1038/378059a0)
31. Ryan MJ, Pease CM, Morris MR. 1992 A genetic polymorphism in the swordtail Xiphophorus nigrensis-testing the prediction of equal fitnesses. Am. Nat. 139, 21-31. (doi:10.1086/285311)
32. Shuster SM, Wade MJ. 1991 Equal mating success among male reproductive strategies in a marine isopod. Nature 350, 608-610. (doi:10.1038/ 350608a0)
33. Emlen DJ. 1994 Environmental control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera, Scarabaeidae). Proc. R. Soc. Lond. B 256, 131-136. (doi:10.1098/rspb. 1994.0060)
34. Kempenaers B, Verheyren GR, Dhondt AA. 1997 Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav. Ecol. 8, 481-492. (doi:10.1093/ beheco/8.5.481)
35. Badyaev AV, Hill GE. 2002 Paternal care as a conditional strategy: distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch. Behav. Ecol. 13, 591-597. (doi:10.1093/beheco/13.5.591)
36. Mitchell DP, Dunn PO, Whittingham LA, Freeman- Gallant CR. 2007 Attractive males provide less parental care in two populations of the common yellowthroat. Anim. Behav. 73, 165-170. (doi:10. 1016/j.anbehav.2006.07.006)
37. Burley NT, Parker PG, Lundy K. 1996 Sexual selection and extrapair fertilization in a socially monogamous passerine, the zebra finch (Taeniopygia guttata). Behav. Ecol. 7, 218-226. (doi:10.1093/beheco/7.2.218)
38. Duckworth RA, Badyaev AV, Parlow AF. 2003 Elaborately ornamented males avoid costly parental care in the house finch (Carpodacus mexicanus): a proximate perspective. Behav. Ecol. Sociobiol. 55, 176-183. (doi:10.1007/s00265-003- 0671-7)
39. Lindstrom J. 1999 Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343-348. (doi:10.1016/S0169-5347(99)01639-0)
40. Burley N, Coopersmith CB. 1987 Bill color preferences of zebra finches. Ethology 76, 133-151. (doi:10.1111/j.1439-0310.1987.tb00679.x)
41. Burley NT, Enstrom DA, Chitwood L. 1994 Extra-pair relations in zebra finches-differential male success results from female tactics. Anim. Behav. 48, 1031-1041. (doi:10.1006/anbe.1994.1336)
42. Crino OL, Van Oorschot BK, Johnson EE, Malisch JL, Breuner CW. 2011 Proximity to a high traffic road: glucocorticoid and life history consequences for nestling white-crowned sparrows. Gen. Comp. Endocrinol. 173, 323-332. (doi:10.1016/j.ygcen. 2011.06.001)
43. Mullner A, Linsenmair KE, Wikelski M. 2004 Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol. Conserv. 118, 549-558. (doi:10.1016/ j.biocon.2003.10.003)
44. Love OP, Bird DM, Shutt LJ. 2003 Plasma corticosterone in American kestrel siblings: effects of age, hatching order, and hatching asynchrony. Horm. Behav. 43, 480-488. (doi:10.1016/S0018- 506x(03)00033-3)
45. Saino N, Suffritti C, Martinelli R, Rubolini D, Moller AP. 2003 Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behav. Ecol. 14, 318-325. (doi:10.1093/beheco/14.3.318)
46. Bize P, Stocker A, Jenni-Eiermann S, Gasparini J, Roulin A. 2010 Sudden weather deterioration but not brood size affects baseline corticosterone levels in nestling Alpine swifts. Horm. Behav. 58, 591-598. (doi:10.1016/j.yhbeh.2010.06.020)
47. Spencer KA, Verhulst S. 2007 Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata). Horm. Behav. 51, 273-280. (doi:10.1016/j.yhbeh.2006.11.001)
48. Crino OL, Driscoll SC, Breuner CW. 2014 Corticosterone exposure during development has sustained but not lifelong effects on body size and total and free corticosterone responses in the zebra finch. Gen. Comp. Endocrinol. 196, 123-129. (doi:10.1016/j.ygcen.2013.10.006)
49. Crino OL, Driscoll SC, Ton R, Breuner CW. 2014 Corticosterone exposure during development improves performance on a novel foraging task in zebra finches. Anim. Behav. 91, 27-32. (doi:10. 1016/j.anbehav.2014.02.017)
50. Peig J, Green AJ. 2009 New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 1883-1891. (doi:10.1111/j.1600-0706. 2009.17643.x)
51. Peig J, Green AJ. 2010 The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct. Ecol. 24, 1323- 1332. (doi:10.1111/j.1365-2435.2010.01751.x)
52. Forstmeier W, Schielzeth H, Schneider M, Kempenaers B. 2007 Development of polymorphic microsatellite markers for the zebra finch (Taeniopygia guttata). Mol. Ecol. Notes 7, 1026- 1028. (doi:10.1111/j.1471-8286.2007.01762.x)
53. Behbahaninia H, Butler MW, Toomey MB, McGraw KJ. 2012 Food color preferences against a dark, textured background vary in relation to sex and age in house finches (Carpodacus mexicanus). Behaviour 149, 51-65. (doi:10.1163/156853912X626141)
54. Butler MW, McGraw KJ. 2009 Indoor housing during development affects moult, carotenoid circulation and beak colouration of mallard ducks (Anas platyrhynchos). Avian Biol. Res. 2, 203-211. (doi:10.3184/175815509X12570082777157)
55. Bolund E. 2009. Condition dependence and fitness consequences of sexual traits in zebra finches. PhD thesis, Max Planck Institute of Ornithology, Seeviesen, Germany.
56. Love OP, Williams TD. 2008 The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. Am. Nat. 172, E135-E149. (doi:10.1086/590959).
57. Trivers RL. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man (ed. B Campbell), pp. 136-179. Chicago, IL: Aldine Press.
58. Pianka ER, Parker WS. 1975 Age-specific reproductive tactics. Am. Nat. 109, 453-464. (doi:10.1086/283013)
59. Clutton-Brock TH. 1984 Reproductive effort and terminal investment in iteroparous animals. Am. Nat. 123, 212-229. (doi:10.1086/284198)
60. Stearns SC. 1992 The evolution of life histories. London, UK: Oxford University Press.
61. Tissier ML, Williams TD, Criscuolo F. 2014 Maternal effects underlie ageing costs of growth in the zebra finch (Taeniopygia guttata). PLoS ONE 9, e97705. (doi:10.1371/journal.pone.0097705)
62. Haussmann MF, Longenecker AS, Marchetto NM, Juliano SA, Bowden RM. 2012 Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc. R. Soc. B 279, 1447-1456. (doi:10.1098/rspb. 2011.1913)
63. Brylawski AMZ, Whittingham LA. 2004 An experimental study of mate guarding and paternity in house wrens. Anim. Behav. 68, 1417-1424. (doi:10.1016/j.anbehav.2004.02.016)
64. Johnsen A, Parn H, Fossoy F, Kleven O, Laskemoen T, Lifjeld JT. 2008 Is female promiscuity constrained by the presence of her social mate? An experiment with bluethroats Luscinia svecica. Behav. Ecol. Sociobiol. 62, 1761-1767. (doi:10.1007/s00265- 008-0604-6)
65. Breuner C. 2008 Maternal stress, glucocorticoids, and the maternal/fetal match hypothesis. Horm. Behav. 54, 485-487. (doi:10.1016/j.yhbeh.2008.05.013)
66. Gluckman PD, Hanson MA. 2004 Living with the past: evolution, development, and patterns of disease. Science 305, 1733-1736. (doi:10.1126/ science.1095292)
67. 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. (doi:10. 1016/j.neubiorev.2004.12.002)
68. Sheriff MJ, Love OP. 2013 Determining the adaptive potential of maternal stress. Ecol. Lett. 16, 271-280. (doi:10.1111/Ele.12042)
69. Love OP, McGowan PO, Sheriff MJ. 2013 Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities. Funct. Ecol. 27, 81-92. (doi:10.1111/j.1365- 2435.2012.02040.x)
70. Losdat S, Helfenstein F, Blount JD, Marri V, Maronde L, Richner H. 2013 Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird. Biol. Lett. 9, Artn 20120888. (doi:10.1098/rsbl. 2012.0888)
71. Monaghan P. 2008 Early growth conditions, phenotypic development and environmental change. Phil. Trans. R. Soc. B 363, 1635-1645. (doi:10.1098/rstb.2007.0011).
72. Chin EH, Love OP, Verspoor JJ, Williams TD, Rowley K, Burness G. 2009 Juveniles exposed to embryonic corticosterone have enhanced flight performance. Proc. R. Soc. B 276, 499-505. (doi:10.1098/rspb.2008.1294)
73. Verspoor JJ, Love OP, Rowland E, Chin EH, Williams TD. 2007 Sex-specific development of avian flight performance under experimentally altered rearing conditions. Behav. Ecol. 18, 967-973. (doi:10.1093/beheco/arm089)