Cited by 481Animal Vocal Communication and BehaviorAnimal Behavior and ReproductionAvian ecology and behavior

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Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis"

S., Nowicki, W., Searcy, S., Peters·2002·Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology

DOI 10.1007/s00359-002-0361-3

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Abstract

The nutritional stress hypothesis explains how learned features of song, such as complexity and local dialect structure, can serve as indicators of male quality of interest to females in mate choice. The link between song and quality comes about because the brain structures underlying song learning largely develop during the first few months post-hatching. During this same period, songbirds are likely to be subject to nutritional and other stresses. Only individuals faring well in the face of stress are able to invest the resources in brain development necessary to optimize song learning. Learned features of song thus become reliable indicators of male quality, with reliability maintained by the developmental costs of song. We review the background and assumptions of the nutritional stress hypothesis, and present new experimental data demonstrating an effect of nestling nutrition on nestling growth, brain development, and song learning, providing support for a key prediction of the hypothesis.

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Mate selection—A selection for a handicap
Zahavi, A. (1975) · Journal of Theoretical Biology · doi:10.1016/0022-5193(75)90111-3 · Cited by 5,251
Biological signals as handicaps
Grafen, A. (1990) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80088-8 · Cited by 2,462
Bird song: biological themes and variations
(1996) · Choice Reviews Online · doi:10.5860/choice.33-2735 · Cited by 2,170
Population Studies of Birds
Southern, H. N., & Lack, D. L. (1967) · Journal of Animal Ecology · doi:10.2307/2828 · Cited by 1,763
The evolution of mating preferences and the paradox of the lek
Kirkpatrick, M., & Ryan, M. J. (1991) · Nature · doi:10.1038/350033a0 · Cited by 1,315
Good genes, oxidative stress and condition–dependent sexual signals
von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D., & Wittzell, H. (1999) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1999.0597 · Cited by 885
PATTERNS OF GROWTH IN BIRDS
Ricklefs, R. E. (1968) · Ibis · doi:10.1111/j.1474-919x.1968.tb00058.x · Cited by 878
Plumage coloration is a sexually selected indicator of male quality
Hill, G. E. (1991) · Nature · doi:10.1038/350337a0 · Cited by 839
THE EVOLUTION OF COSTLY MATE PREFERENCES II. THE “HANDICAP” PRINCIPLE
Iwasa, Y., Pomiankowski, A., & Nee, S. (1991) · Evolution · doi:10.1111/j.1558-5646.1991.tb02646.x · Cited by 757
A Brain for All Seasons: Cyclical Anatomical Changes in Song Control Nuclei of the Canary Brain
Nottebohm, F. (1981) · Science · doi:10.1126/science.7313697 · Cited by 753

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(2004) · Elsevier eBooks · doi:10.1016/b978-012473070-0/50018-9
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References
(2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801562-9.09998-1
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Authors: S., N., W., S., & S., P.
Venue: Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology
Publisher: Springer Science and Business Media LLC
Published: 2002-12-01
Volume: 188
Issue: 11-12
Pages: 1003-1014
ISSN: 0340-7594 (ISSN-L)
1432-1351
DOI: 10.1007/s00359-002-0361-3
OpenAlex: W2117191589
Cited by: 481
References: 106
Citations by year: 2026: 7 · 2025: 8 · 2024: 12 · 2023: 5 · 2022: 16 · 2021: 15 · 2020: 13 · 2019: 23 · 2018: 29 · 2017: 26 · 2016: 29 · 2015: 60 · 2014: 29 · 2013: 28 · 2012: 21
FWCI: 9.72
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Journal of Comparative Physiology A (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation
National Institutes of Health
Topics: Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Vocal Communication and Behavior
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Physical Sciences › Environmental Science › Ecology › Avian ecology and behavior
Keywords: song learning, mate choice, song complexity, dialect structure, male quality, nestling growth, sexual selection
MeSH terms: Age Factors, Animals, Birds, Body Weight, Brain, Biological Evolution, Feathers, Female, Learning, Male, Nutritional Physiological Phenomena, Sex, Sound Spectrography, Stress, Physiological, Telencephalon, Vocalization, Animal, Voice, Prosencephalon, Statistics, Nonparametric

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Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis"

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