Early-life stress affects song complexity, song learning and volume of the brain nucleus RA in adult male song sparrows

Animal Behaviour

Volumn 86, Issue 1, 2013, Pages 25-35

  Schmidt, Kim L ^a   Moore, S Drew ^a   MacDougall Shackleton, Elizabeth A ^a   MacDougall Shackleton, Scott A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Developmental indicator; Glucocorticoid; Melospiza melodia; Nutritional stress; Sexual selection; Song control system; Song sparrow; Songbird; Vocal performance

Indexed keywords

ADULT; ANATOMY; BIOLOGICAL DEVELOPMENT; BRAIN; ENVIRONMENTAL STRESS; HONEST SIGNALING; HYPOTHESIS TESTING; LEARNING; NEUROLOGY; NUTRIENT AVAILABILITY; ONTOGENY; SONG; SONGBIRD; VOCALIZATION;

AVES; MELOSPIZA; MELOSPIZA MELODIA; PASSERI;

EID: 84880167873     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2013.03.036     Document Type: Article

References (72)

1. Airey D.C., DeVoogd T.J. Greater song complexity is associated with augmented song system anatomy in zebra finches. Neuroreport 2000, 11:2339-2344.
2. Ballentine H.J. The ability to perform physically challenging songs predicts age and size in male swamp sparrows, Melospiza georgiana. Animal Behaviour 2009, 77:973-978.
3. Ballentine H., Hyman J., Nowicki S. Vocal performance influences female response to male bird song: an experimental test. Behavioral Ecology 2004, 15:163-168.
4. Beecher M.D., Burt M.J. The role of social interaction in bird song learning. Current Directions in Psychological Sciences 2004, 13:224-228.
5. Beecher M.D., Campbell E., Nordby J.C. Territory tenure in song sparrows is related to song sharing with neighbours, but not to repertoire size. Animal Behaviour 2000, 59:29-37.
6. Bennis-Taleb N., Remacle C., Hoet J.J., Reusens B. Alow-protein isocaloric diet during gestation affects brain development and alters permanently cerebral cortex blood vessels in rat offspring. Journal of Nutrition 1999, 129:1613-1619.
7. Bernard D.J., Eens M., Ball G.F. Age- and behavior-related variation in volumes of song control nuclei in male European starlings. Journal of Neurobiology 1996, 30:329-339.
8. Blackburn T.M., Lawton J.H., Perry J.N. Amethod of estimating the slope of upper bounds of plots of body size and abundance in natural animal assemblages. Oikos 1992, 65:107-112.
9. Bottjer S.W., Glaessner S.L., Arnold A.P. Ontogeny of brain nuclei controlling song learning and behavior in zebra finches. Journal of Neuroscience 1985, 5:1556-1562.
10. Bottjer S.W., Miesner E.A., Arnold A.P. Changes in neuronal number, density and size account for increases in volume of song-control nuclei during song development in zebra finches. Neuroscience Letters 1986, 67:263-268.
11. Brumm H., Zollinger S.A., Slater P.J.B. Developmental stress affects song learning but not song complexity and vocal amplitude in zebra finches. Behavioral Ecology and Sociobiology 2009, 63:1387-1395.
12. Buchanan K.L., Catchpole C.K. Song as an indicator of male parental effort in the sedge warbler. Proceedings of the Royal Society B 2000, 267:321-326.
13. Buchanan K.L., Spencer K.A., Goldsmith A.R., Catchpole C.K. Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proceedings of the Royal Society B 2003, 270:1149-1156.
14. Buchanan K.L., Leitner S., Spencer K.A., Goldsmith A.R., Catchpole C.K. Developmental stress selectively affects the song control nucleus HVC in the zebra finch. Proceedings of the Royal Society B 2004, 271:2381-2386.
15. Catchpole C.K., Slater P.J.B. Bird Song: Biological Themes and Variations 1995, Cambridge University Press, Cambridge.
16. DeVoogd T.J., Krebs J.R., Healy S.D., Purvis A. Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds. Proceedings of the Royal Society B 1993, 254:75-82.
17. Farrell T.M., Weaver K., An Y.S., MacDougall-Shackleton S.A. Song bout length is indicative of spatial learning in European starlings. Behavioral Ecology 2011, 23:101-111.
18. Gallagher E.A., Newman J.P., Green L.R., Hanson M.A. The effect of low protein diet in pregnancy on the development of brain metabolism in rat offspring. Journal of Physiology 2005, 568:553-558.
19. Garamszegi L.Z., Eens M. Brain space for a learned task: strong intraspecific evidence for neural correlates of singing behavior in songbirds. Brain Research Reviews 2004, 44:187-193.
20. Gil D., Leboucher G., Lacroix A., Cue R., Kreutzer M. Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Hormones and Behavior 2004, 45:64-70.
21. Glasser J., Greene G., Hendricks S. Stereology for Biological Research: with a Focus on Neuroscience 2007, MBF Press, Williston, Vermont.
22. Gluckman P.D., Hanson M.A., Spencer H.G., Bateson P. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proceedings of the Royal Society B 2005, 272:671-677.
23. Gressens P., Muaku S.M., Besse L., Nsegbe E., Gallego J., Delpech B., Gaultier C., Evrard P., Ketelslegers J.M., Maiter D. Maternal protein restriction early in rat pregnancy alters brain development in the progeny. Developmental Brain Research 1997, 103:21-35.
24. Griffiths R., Double M.C., Orr K., Dawson R.J. ADNA test to sex most birds. Molecular Ecology 1998, 7:1071-1075.
25. Hales C.N., Ozanne S.E. The dangerous road of catch-up growth. Journal of Physiology 2003, 547:5-10.
26. Hall Z.J., MacDougall-Shackleton S.A. Influence of testosterone metabolites on song-control system neuroplasticity during photostimulation in adult European starlings (Sturnus vulgaris). PLoS One 2012, 7. e40060.
27. Hiebert S.M., Stoddard P.K., Arcese P. Repertoire size, territory acquisition and reproductive success in the song sparrow. Animal Behaviour 1989, 37:266-273.
28. Kempster B., Zanette L., Longstaffe F.J., MacDougall-Shackleton S.A., Wingfield J.C., Clinchy M. Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 2007, 151:365-371.
29. Kirn J.R., Clower R.P., Kroodsma D.E., DeVoogd T.J. Song-related brain regions in the red-winged blackbird are affected by sex and season but not repertoire size. Journal of Neurobiology 1989, 20:139-163.
30. Kitaysky A.S., Kitaiskaia E.V., Wingfield J.C., Piatt J.F. Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. Journal of Comparative Physiology B 2001, 171:701-709.
31. Laus M.F., Vales L.D., Costa T.M., Almeida S.S. Early postnatal protein-calorie malnutrition and cognition: a review of human and animal studies. International Journal of Environmental Research and Public Health 2011, 8:590-612.
32. Leitner S., Marshall R.C., Leisler B., Catchpole C.K. Male song quality, egg size and offspring sex in captive canaries (Serinus canaria). Ethology 2006, 112:554-563.
33. Lesage J., Blondeau B., Grino M., Breant B., Dupouy J.P. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology 2001, 142:1692-1702.
34. MacDonald I.F., Kempster B., Zanette L., MacDougall-Shackleton S.A. Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning. Proceedings of the Royal Society B 2006, 273:2559-2564.
35. MacDougall-Shackleton S.A. Sexual selection and the evolution of song repertoires. Current Ornithology 1997, 14:81-124.
36. MacDougall-Shackleton S.A., Spencer K.A. Developmental stress and birdsong: current evidence and future directions. Journal of Ornithology 2012, 153:105-117.
37. MacDougall-Shackleton S.A., Hulse S.H., Ball G.F. Neural correlates of singing behavior in male zebra finches (Taeniopygia guttata). Journal of Neurobiology 1998, 36:421-430.
38. MacDougall-Shackleton S.A., MacDougall-Shackleton E.A., Hahn T.P. Physiological and behavioral responses of female mountain white-crowned sparrows to natal- and foreign-dialect songs. Canadian Journal of Zoology 2001, 79:325-333.
39. Marler P., Peters S. Asensitive period for song acquisition in the song sparrow, Melospiza melodia: a case of age-limited learning. Ethology 1987, 76:89-100.
40. Metcalfe N.B., Monaghan P. Compensation for a bad start: grow now, pay later?. Trends in Ecology & Evolution 2001, 16:254-260.
41. Møller A.P., Pomiankowski A. Why have birds got multiple sexual ornaments?. Behavioral Ecology and Sociobiology 1993, 32:167-176.
42. Mooney R., Rao M. Waiting periods versus early innervation: the development of axonal connections in the zebra finch song system. Journal of Neuroscience 1994, 14:6532-6543.
43. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
44. Newman A.E., MacDougall-Shackleton S.A., An Y.S., Kriengwatana B., Soma K.K. Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the avian song control system. Journal of Comparative Neurology 2010, 518:3662-3678.
45. Nordby J.C., Campbell S.E., Beecher M.D. Late song learning in song sparrows. Animal Behaviour 2001, 61:835-846.
46. Nordby J.C., Campbell E.C., Beecher M.D. Adult song sparrows do not alter their song repertoires. Ethology 2002, 108:39-50.
47. Nowicki S., Searcy W.A. Song function and the evolution of female preferences: why birds sing, why brains matter. Annals of the New York Academy of Sciences 2004, 1016:704-723.
48. Nowicki S., Peters S., Podos J. Song learning, early nutrition and sexual selection in songbirds. Integrative and Comparative Biology 1998, 38:179-190.
49. Nowicki S., Searcy W.A., Peters S. Quality of song learning affects female response to male bird song. Proceedings of the Royal Society B 2002, 269:1949-1954.
50. Nowicki S., Searcy W.A., Peters S. Brain development, song learning and mate choice in birds: a review and experimental test of the 'nutritional stress hypothesis'. Journal of Comparative Physiology A 2002, 188:1003-1014.
51. Pfaff J.A., Zanette L., MacDougall-Shackleton S.A., MacDougall-Shackleton E.A. Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia). Proceedings of the Royal Society B 2007, 274:2035-2040.
52. Philmore L.S., Hoshooley J.S., Sherry D.S., MacDougall-Shackleton S.A. Annual cycle of the black-capped chickadee: seasonality of singing rates and vocal-control brain regions. Journal of Neurobiology 2006, 66:1002-1010.
53. Podos J. Aperformance constraint on the evolution of trilled vocalizations in a songbird family (Passeriformes: Emberizidae). Evolution 1997, 51:537-551.
54. Podos J. Corelated evolution of morphology and vocal signal structure in Darwin's finches. Nature 2001, 409:185-188.
55. Podos J., Lahti D.C., Moseley D.L. Vocal performance and sensorimotor learning in songbirds. Advances in the Study of Behavior 2009, 40:159-195.
56. Potvin D.A., MacDougall-Shackleton E.A. Parental investment amplifies effects of genetic complementarity on growth rates in song sparrows, Melospiza melodia. Animal Behaviour 2009, 78:943-948.
57. Reid J.M., Arcese P., Cassidy A.L.E.V., Hiebert S.M., Smith J.N.M., Stoddard P.K., Marr A.B., Keller L.F. Song repertoire size predicts initial mating success in male song sparrows, Melospiza melodia. Animal Behaviour 2004, 68:1055-1063.
58. Schmidt K.L., MacDougall-Shackleton E.A., Macdougall-Shackleton S.A. 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. Journal of Experimental Biology 2012, 215:3207-3217.
59. Searcy W.A. Song repertoire size and female preferences in song sparrows. Behavioral Ecology and Sociobiology 1984, 14:281-286.
60. Simons S.D., Johnston P.V. Prenatal and postnatal protein restriction in the rat: effect on some parameters related to brain development, and prospects for rehabilitation. Journal of Neurochemistry 1976, 27:63-69.
61. Smith G.T., Brenowitz E.A., Beecher M.D., Wingfield J.C. Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. Journal of Neuroscience 1997, 17:6001-6010.
62. Smith G.T., Brenowitz E.A., Wingfield J.C. Seasonal changes in the size of the avian song control nucleus HVC defined by multiple histological markers. Journal of Comparative Neurology 1997, 381:253-261.
63. Sockman K.W. Annual variation in vocal performance and its relationship with bill morphology in Lincoln's sparrows. Animal Behaviour 2009, 77:663-671.
64. Spencer K.A., MacDougall-Shackleton S.A. Indicators of development as sexually selected traits: the developmental stress hypothesis in context. Behavioral Ecology 2011, 22:1-9.
65. Spencer K.A., Buchanan K.L., Goldsmith A.R., Catchpole C.K. Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Hormones and Behavior 2003, 44:132-139.
66. Spencer K.A., Buchanan K.L., Goldsmith A.R., Catchpole C.K. Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris). Proceedings of the Royal Society B, Supplement 2004, 271:S121-S123.
67. Spencer K.A., Evans N.P., Monaghan P. Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology 2009, 150:1931-1934.
68. Stewart K.A., MacDougall-Shackleton E.A. Local song elements indicate local genotypes and predict physiological condition in song sparrows Melospiza melodia. Biology Letters 2008, 4:240-242.
69. Tramontin A.D., Hartman V.N., Brenowitz E.A. Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain. Journal of Neuroscience 2000, 20:854-861.
70. Verhulst S., Holveck M.-J., Riebel K. Long-term effects of manipulated natal brood size on metabolic rate in zebra finches. Biology Letters 2006, 2:478-480.
71. Welberg L.A., Seckl J.R. Prenatal stress, glucocorticoids and the programming of the brain. Journal of Neuroendocrinology 2001, 13:113-128.
72. Williams T.D. Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biological Reviews 1994, 69:35-59.