Oxidative stress and the effect of parasites on a carotenoid-based ornament

Francois Robert Mougeot, Jesus Martinez-Padilla, J. D. Blount, Lorenzo Perez-Rodriguez, L.M.I Webster, Stuart Brannon Piertney

Research output: Contribution to journalArticle

43 Citations (Scopus)

Abstract

Oxidative stress, the physiological condition whereby the production of reactive oxygen and nitrogen species overwhelms the capacity of antioxidant defences, causes damage to key bio-molecules. It has been implicated in many diseases, and is proposed as a reliable currency in the trade-off between individual health and ornamentation. Whether oxidative stress mediates the expression of carotenoid-based signals, which are among the commonest signals of many birds, fish and reptiles, remains controversial. In the present study, we explored interactions between parasites, oxidative stress and the carotenoid-based ornamentation of red grouse Lagopus lagopus scoticus. We tested whether removing nematode parasites influenced both oxidative balance (levels of oxidative damage and circulating antioxidant defences) and carotenoid-based ornamentation. At the treatment group level, parasite purging enhanced the size and colouration of ornaments but did not significantly affect circulating carotenoids, antioxidant defences or oxidative damage. However, relative changes in these traits among individuals indicated that males with a greater number of parasites prior to treatment (parasite purging) showed a greater increase in the levels of circulating carotenoids and antioxidants, and a greater decrease in oxidative damage, than those with initially fewer parasites. At the individual level, a greater increase in carotenoid pigmentation was associated with a greater reduction in oxidative damage. Therefore, an individual's ability to express a carotenoid-based ornament appeared to be linked to its current oxidative balance and susceptibility to oxidative stress. Our experimental results suggest that oxidative stress can mediate the impact of parasites on carotenoid-based signals, and we discuss possible mechanisms linking carotenoid-based ornaments to oxidative stress.

Original languageEnglish
Pages (from-to)400-407
Number of pages8
JournalJournal of Experimental Biology
Volume213
Issue number3
Early online date19 Jan 2010
DOIs
Publication statusPublished - 1 Feb 2010

Keywords

  • lipid peroxidation
  • oxidative damage
  • antioxidant defences
  • honest signalling
  • nematode Trichostrongylus tenuis
  • red grouse Lagopus lagopus scoticus
  • sexual selection
  • LAGOPUS-LAGOPUS-SCOTICUS
  • MALE RED GROUSE
  • AUTUMN TERRITORIAL BEHAVIOR
  • MALE HOUSE FINCHES
  • IMMUNE ACTIVATION
  • PLUMAGE COLORATION
  • SEXUAL SIGNALS
  • BIOLOGICAL SAMPLES
  • ALECTORIS-RUFA
  • ZEBRA FINCHES
  • nematode Trichostrongylus tenuis

Cite this

Mougeot, F. R., Martinez-Padilla, J., Blount, J. D., Perez-Rodriguez, L., Webster, L. M. I., & Piertney, S. B. (2010). Oxidative stress and the effect of parasites on a carotenoid-based ornament. Journal of Experimental Biology, 213(3), 400-407. https://doi.org/10.1242/jeb.037101

Oxidative stress and the effect of parasites on a carotenoid-based ornament. / Mougeot, Francois Robert; Martinez-Padilla, Jesus; Blount, J. D.; Perez-Rodriguez, Lorenzo; Webster, L.M.I ; Piertney, Stuart Brannon.

In: Journal of Experimental Biology, Vol. 213, No. 3, 01.02.2010, p. 400-407.

Research output: Contribution to journalArticle

Mougeot, FR, Martinez-Padilla, J, Blount, JD, Perez-Rodriguez, L, Webster, LMI & Piertney, SB 2010, 'Oxidative stress and the effect of parasites on a carotenoid-based ornament' Journal of Experimental Biology, vol. 213, no. 3, pp. 400-407. https://doi.org/10.1242/jeb.037101
Mougeot FR, Martinez-Padilla J, Blount JD, Perez-Rodriguez L, Webster LMI, Piertney SB. Oxidative stress and the effect of parasites on a carotenoid-based ornament. Journal of Experimental Biology. 2010 Feb 1;213(3):400-407. https://doi.org/10.1242/jeb.037101
Mougeot, Francois Robert ; Martinez-Padilla, Jesus ; Blount, J. D. ; Perez-Rodriguez, Lorenzo ; Webster, L.M.I ; Piertney, Stuart Brannon. / Oxidative stress and the effect of parasites on a carotenoid-based ornament. In: Journal of Experimental Biology. 2010 ; Vol. 213, No. 3. pp. 400-407.
@article{f7e21bb99ef94f0992cfd291f2e5553f,
title = "Oxidative stress and the effect of parasites on a carotenoid-based ornament",
abstract = "Oxidative stress, the physiological condition whereby the production of reactive oxygen and nitrogen species overwhelms the capacity of antioxidant defences, causes damage to key bio-molecules. It has been implicated in many diseases, and is proposed as a reliable currency in the trade-off between individual health and ornamentation. Whether oxidative stress mediates the expression of carotenoid-based signals, which are among the commonest signals of many birds, fish and reptiles, remains controversial. In the present study, we explored interactions between parasites, oxidative stress and the carotenoid-based ornamentation of red grouse Lagopus lagopus scoticus. We tested whether removing nematode parasites influenced both oxidative balance (levels of oxidative damage and circulating antioxidant defences) and carotenoid-based ornamentation. At the treatment group level, parasite purging enhanced the size and colouration of ornaments but did not significantly affect circulating carotenoids, antioxidant defences or oxidative damage. However, relative changes in these traits among individuals indicated that males with a greater number of parasites prior to treatment (parasite purging) showed a greater increase in the levels of circulating carotenoids and antioxidants, and a greater decrease in oxidative damage, than those with initially fewer parasites. At the individual level, a greater increase in carotenoid pigmentation was associated with a greater reduction in oxidative damage. Therefore, an individual's ability to express a carotenoid-based ornament appeared to be linked to its current oxidative balance and susceptibility to oxidative stress. Our experimental results suggest that oxidative stress can mediate the impact of parasites on carotenoid-based signals, and we discuss possible mechanisms linking carotenoid-based ornaments to oxidative stress.",
keywords = "lipid peroxidation, oxidative damage, antioxidant defences, honest signalling, nematode Trichostrongylus tenuis, red grouse Lagopus lagopus scoticus, sexual selection, LAGOPUS-LAGOPUS-SCOTICUS, MALE RED GROUSE, AUTUMN TERRITORIAL BEHAVIOR, MALE HOUSE FINCHES, IMMUNE ACTIVATION, PLUMAGE COLORATION, SEXUAL SIGNALS, BIOLOGICAL SAMPLES, ALECTORIS-RUFA, ZEBRA FINCHES, nematode Trichostrongylus tenuis",
author = "Mougeot, {Francois Robert} and Jesus Martinez-Padilla and Blount, {J. D.} and Lorenzo Perez-Rodriguez and L.M.I Webster and Piertney, {Stuart Brannon}",
year = "2010",
month = "2",
day = "1",
doi = "10.1242/jeb.037101",
language = "English",
volume = "213",
pages = "400--407",
journal = "Journal of Experimental Biology",
issn = "0022-0949",
publisher = "Company of Biologists Ltd",
number = "3",

}

TY - JOUR

T1 - Oxidative stress and the effect of parasites on a carotenoid-based ornament

AU - Mougeot, Francois Robert

AU - Martinez-Padilla, Jesus

AU - Blount, J. D.

AU - Perez-Rodriguez, Lorenzo

AU - Webster, L.M.I

AU - Piertney, Stuart Brannon

PY - 2010/2/1

Y1 - 2010/2/1

N2 - Oxidative stress, the physiological condition whereby the production of reactive oxygen and nitrogen species overwhelms the capacity of antioxidant defences, causes damage to key bio-molecules. It has been implicated in many diseases, and is proposed as a reliable currency in the trade-off between individual health and ornamentation. Whether oxidative stress mediates the expression of carotenoid-based signals, which are among the commonest signals of many birds, fish and reptiles, remains controversial. In the present study, we explored interactions between parasites, oxidative stress and the carotenoid-based ornamentation of red grouse Lagopus lagopus scoticus. We tested whether removing nematode parasites influenced both oxidative balance (levels of oxidative damage and circulating antioxidant defences) and carotenoid-based ornamentation. At the treatment group level, parasite purging enhanced the size and colouration of ornaments but did not significantly affect circulating carotenoids, antioxidant defences or oxidative damage. However, relative changes in these traits among individuals indicated that males with a greater number of parasites prior to treatment (parasite purging) showed a greater increase in the levels of circulating carotenoids and antioxidants, and a greater decrease in oxidative damage, than those with initially fewer parasites. At the individual level, a greater increase in carotenoid pigmentation was associated with a greater reduction in oxidative damage. Therefore, an individual's ability to express a carotenoid-based ornament appeared to be linked to its current oxidative balance and susceptibility to oxidative stress. Our experimental results suggest that oxidative stress can mediate the impact of parasites on carotenoid-based signals, and we discuss possible mechanisms linking carotenoid-based ornaments to oxidative stress.

AB - Oxidative stress, the physiological condition whereby the production of reactive oxygen and nitrogen species overwhelms the capacity of antioxidant defences, causes damage to key bio-molecules. It has been implicated in many diseases, and is proposed as a reliable currency in the trade-off between individual health and ornamentation. Whether oxidative stress mediates the expression of carotenoid-based signals, which are among the commonest signals of many birds, fish and reptiles, remains controversial. In the present study, we explored interactions between parasites, oxidative stress and the carotenoid-based ornamentation of red grouse Lagopus lagopus scoticus. We tested whether removing nematode parasites influenced both oxidative balance (levels of oxidative damage and circulating antioxidant defences) and carotenoid-based ornamentation. At the treatment group level, parasite purging enhanced the size and colouration of ornaments but did not significantly affect circulating carotenoids, antioxidant defences or oxidative damage. However, relative changes in these traits among individuals indicated that males with a greater number of parasites prior to treatment (parasite purging) showed a greater increase in the levels of circulating carotenoids and antioxidants, and a greater decrease in oxidative damage, than those with initially fewer parasites. At the individual level, a greater increase in carotenoid pigmentation was associated with a greater reduction in oxidative damage. Therefore, an individual's ability to express a carotenoid-based ornament appeared to be linked to its current oxidative balance and susceptibility to oxidative stress. Our experimental results suggest that oxidative stress can mediate the impact of parasites on carotenoid-based signals, and we discuss possible mechanisms linking carotenoid-based ornaments to oxidative stress.

KW - lipid peroxidation

KW - oxidative damage

KW - antioxidant defences

KW - honest signalling

KW - nematode Trichostrongylus tenuis

KW - red grouse Lagopus lagopus scoticus

KW - sexual selection

KW - LAGOPUS-LAGOPUS-SCOTICUS

KW - MALE RED GROUSE

KW - AUTUMN TERRITORIAL BEHAVIOR

KW - MALE HOUSE FINCHES

KW - IMMUNE ACTIVATION

KW - PLUMAGE COLORATION

KW - SEXUAL SIGNALS

KW - BIOLOGICAL SAMPLES

KW - ALECTORIS-RUFA

KW - ZEBRA FINCHES

KW - nematode Trichostrongylus tenuis

U2 - 10.1242/jeb.037101

DO - 10.1242/jeb.037101

M3 - Article

VL - 213

SP - 400

EP - 407

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 3

ER -