Physiological stress mediates the honesty of social signals

Gary R Bortolotti, Francis Mougeot, Jesus Martinez-Padilla, Lucy M I Webster, Stuart B Piertney

Research output: Contribution to journalArticle

70 Citations (Scopus)
3 Downloads (Pure)

Abstract

Background: Extravagant ornaments used as social signals evolved to advertise their bearers' quality. The Immunocompetence Handicap Hypothesis proposes that testosterone-dependent ornaments reliably signal health and parasite resistance; however, empirical studies have shown mixed support. Alternatively, immune function and parasite resistance may be indirectly or directly related to glucocorticoid stress hormones. We propose that an understanding of the interplay between the individual and its environment, particularly how they cope with stressors, is crucial for understanding the honesty of social signals.

Methodology/Principal Findings: We analyzed corticosterone deposited in growing feathers as an integrated measure of hypothalamic-pituitary-adrenal activity in a wild territorial bird, the red grouse Lagopus lagopus scoticus. We manipulated two key, interrelated components, parasites and testosterone, which influence both ornamentation and fitness. Birds were initially purged of parasites, and later challenged with parasites or not, while at the same time being given testosterone or control implants, using a factorial experimental design. At the treatment level, testosterone enhanced ornamentation, while parasites reduced it, but only in males not implanted with testosterone. Among individuals, the degree to which both parasites and testosterone had an effect was strongly dependent on the amount of corticosterone in the feather grown during the experiment. The more stressors birds had experienced (i.e., higher corticosterone), the more parasites developed, and the less testosterone enhanced ornamentation.

Conclusions/Significance: With this unique focus on the individual, and a novel, integrative, measure of response to stressors, we show that ornamentation is ultimately a product of the cumulative physiological response to environmental challenges. These findings lead toward a more realistic concept of honesty in signaling as well as a broader discussion of the concept of stress.

Original languageEnglish
Article numbere4893
Number of pages8
JournalPloS ONE
Volume4
Issue number3
DOIs
Publication statusPublished - 25 Mar 2009

Keywords

  • lagopus-lagopus-scoticus
  • male red grouse
  • immunocompetence handicap hypothesis
  • autumn territorial behavior
  • trichostrongylus-tenuis
  • plumage coloration
  • immune function
  • zebra finches
  • trade-offs
  • testosterone

Cite this

Bortolotti, G. R., Mougeot, F., Martinez-Padilla, J., Webster, L. M. I., & Piertney, S. B. (2009). Physiological stress mediates the honesty of social signals. PloS ONE, 4(3), [e4893]. https://doi.org/10.1371/journal.pone.0004983

Physiological stress mediates the honesty of social signals. / Bortolotti, Gary R; Mougeot, Francis; Martinez-Padilla, Jesus; Webster, Lucy M I; Piertney, Stuart B.

In: PloS ONE, Vol. 4, No. 3, e4893, 25.03.2009.

Research output: Contribution to journalArticle

Bortolotti, GR, Mougeot, F, Martinez-Padilla, J, Webster, LMI & Piertney, SB 2009, 'Physiological stress mediates the honesty of social signals' PloS ONE, vol. 4, no. 3, e4893. https://doi.org/10.1371/journal.pone.0004983
Bortolotti GR, Mougeot F, Martinez-Padilla J, Webster LMI, Piertney SB. Physiological stress mediates the honesty of social signals. PloS ONE. 2009 Mar 25;4(3). e4893. https://doi.org/10.1371/journal.pone.0004983
Bortolotti, Gary R ; Mougeot, Francis ; Martinez-Padilla, Jesus ; Webster, Lucy M I ; Piertney, Stuart B. / Physiological stress mediates the honesty of social signals. In: PloS ONE. 2009 ; Vol. 4, No. 3.
@article{689e766dca3a49ad85d0d37510561f3a,
title = "Physiological stress mediates the honesty of social signals",
abstract = "Background: Extravagant ornaments used as social signals evolved to advertise their bearers' quality. The Immunocompetence Handicap Hypothesis proposes that testosterone-dependent ornaments reliably signal health and parasite resistance; however, empirical studies have shown mixed support. Alternatively, immune function and parasite resistance may be indirectly or directly related to glucocorticoid stress hormones. We propose that an understanding of the interplay between the individual and its environment, particularly how they cope with stressors, is crucial for understanding the honesty of social signals. Methodology/Principal Findings: We analyzed corticosterone deposited in growing feathers as an integrated measure of hypothalamic-pituitary-adrenal activity in a wild territorial bird, the red grouse Lagopus lagopus scoticus. We manipulated two key, interrelated components, parasites and testosterone, which influence both ornamentation and fitness. Birds were initially purged of parasites, and later challenged with parasites or not, while at the same time being given testosterone or control implants, using a factorial experimental design. At the treatment level, testosterone enhanced ornamentation, while parasites reduced it, but only in males not implanted with testosterone. Among individuals, the degree to which both parasites and testosterone had an effect was strongly dependent on the amount of corticosterone in the feather grown during the experiment. The more stressors birds had experienced (i.e., higher corticosterone), the more parasites developed, and the less testosterone enhanced ornamentation. Conclusions/Significance: With this unique focus on the individual, and a novel, integrative, measure of response to stressors, we show that ornamentation is ultimately a product of the cumulative physiological response to environmental challenges. These findings lead toward a more realistic concept of honesty in signaling as well as a broader discussion of the concept of stress.",
keywords = "lagopus-lagopus-scoticus, male red grouse, immunocompetence handicap hypothesis, autumn territorial behavior, trichostrongylus-tenuis, plumage coloration, immune function, zebra finches, trade-offs, testosterone",
author = "Bortolotti, {Gary R} and Francis Mougeot and Jesus Martinez-Padilla and Webster, {Lucy M I} and Piertney, {Stuart B}",
year = "2009",
month = "3",
day = "25",
doi = "10.1371/journal.pone.0004983",
language = "English",
volume = "4",
journal = "PloS ONE",
issn = "1932-6203",
publisher = "PUBLIC LIBRARY SCIENCE",
number = "3",

}

TY - JOUR

T1 - Physiological stress mediates the honesty of social signals

AU - Bortolotti, Gary R

AU - Mougeot, Francis

AU - Martinez-Padilla, Jesus

AU - Webster, Lucy M I

AU - Piertney, Stuart B

PY - 2009/3/25

Y1 - 2009/3/25

N2 - Background: Extravagant ornaments used as social signals evolved to advertise their bearers' quality. The Immunocompetence Handicap Hypothesis proposes that testosterone-dependent ornaments reliably signal health and parasite resistance; however, empirical studies have shown mixed support. Alternatively, immune function and parasite resistance may be indirectly or directly related to glucocorticoid stress hormones. We propose that an understanding of the interplay between the individual and its environment, particularly how they cope with stressors, is crucial for understanding the honesty of social signals. Methodology/Principal Findings: We analyzed corticosterone deposited in growing feathers as an integrated measure of hypothalamic-pituitary-adrenal activity in a wild territorial bird, the red grouse Lagopus lagopus scoticus. We manipulated two key, interrelated components, parasites and testosterone, which influence both ornamentation and fitness. Birds were initially purged of parasites, and later challenged with parasites or not, while at the same time being given testosterone or control implants, using a factorial experimental design. At the treatment level, testosterone enhanced ornamentation, while parasites reduced it, but only in males not implanted with testosterone. Among individuals, the degree to which both parasites and testosterone had an effect was strongly dependent on the amount of corticosterone in the feather grown during the experiment. The more stressors birds had experienced (i.e., higher corticosterone), the more parasites developed, and the less testosterone enhanced ornamentation. Conclusions/Significance: With this unique focus on the individual, and a novel, integrative, measure of response to stressors, we show that ornamentation is ultimately a product of the cumulative physiological response to environmental challenges. These findings lead toward a more realistic concept of honesty in signaling as well as a broader discussion of the concept of stress.

AB - Background: Extravagant ornaments used as social signals evolved to advertise their bearers' quality. The Immunocompetence Handicap Hypothesis proposes that testosterone-dependent ornaments reliably signal health and parasite resistance; however, empirical studies have shown mixed support. Alternatively, immune function and parasite resistance may be indirectly or directly related to glucocorticoid stress hormones. We propose that an understanding of the interplay between the individual and its environment, particularly how they cope with stressors, is crucial for understanding the honesty of social signals. Methodology/Principal Findings: We analyzed corticosterone deposited in growing feathers as an integrated measure of hypothalamic-pituitary-adrenal activity in a wild territorial bird, the red grouse Lagopus lagopus scoticus. We manipulated two key, interrelated components, parasites and testosterone, which influence both ornamentation and fitness. Birds were initially purged of parasites, and later challenged with parasites or not, while at the same time being given testosterone or control implants, using a factorial experimental design. At the treatment level, testosterone enhanced ornamentation, while parasites reduced it, but only in males not implanted with testosterone. Among individuals, the degree to which both parasites and testosterone had an effect was strongly dependent on the amount of corticosterone in the feather grown during the experiment. The more stressors birds had experienced (i.e., higher corticosterone), the more parasites developed, and the less testosterone enhanced ornamentation. Conclusions/Significance: With this unique focus on the individual, and a novel, integrative, measure of response to stressors, we show that ornamentation is ultimately a product of the cumulative physiological response to environmental challenges. These findings lead toward a more realistic concept of honesty in signaling as well as a broader discussion of the concept of stress.

KW - lagopus-lagopus-scoticus

KW - male red grouse

KW - immunocompetence handicap hypothesis

KW - autumn territorial behavior

KW - trichostrongylus-tenuis

KW - plumage coloration

KW - immune function

KW - zebra finches

KW - trade-offs

KW - testosterone

U2 - 10.1371/journal.pone.0004983

DO - 10.1371/journal.pone.0004983

M3 - Article

VL - 4

JO - PloS ONE

JF - PloS ONE

SN - 1932-6203

IS - 3

M1 - e4893

ER -