Nematode parasites reduce carotenoid-based signalling in male red grouse

Martínez‐Padilla, Jesús; Mougeot, François; Pérez‐Rodríguez, Lorenzo; Bortolotti, Gary R.

doi:10.1098/rsbl.2006.0593

Cited by 81 publications

(78 citation statements)

References 19 publications

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“…These findings support the idea that sexual displays may signal male infection status as already observed in some biological models (e.g. Hill & Brawner 1998;Brawner et al 2000;Horak et al 2004;Martinez-Padilla et al 2007). Previous studies, including in blackbirds, that used antigenic challenges provided direct support for the idea that immune defences and sexual signals compete for carotenoids (Blount et al 2003;Faivre et al 2003).…”

Section: Discussionsupporting

confidence: 87%

“…In addition, previous experimental studies using parasites have found that (i) controlled infections reduce the expression of carotenoid-based ornamentation (Hill & Brawner 1998;Brawner et al 2000;Horak et al 2004), (ii) parasite eradication positively affects carotenoidbased ornamentation (Martinez-Padilla et al 2007), and (iii) expression level of ornaments may indicate males' ability to clear parasite infection (Lindströ m & Lundström 2000). Furthermore, newly developed methods, which allow measurement of the magnitude of the immune response to various antigens (see Adamo (2004) for a review), made it possible to identify a positive relationship between carotenoid-based coloration and various immune effectors (Blount et al 2003;McGraw & Ardia 2003 and references therein), and have also shown that immune defence and sexual attractiveness are constrained by carotenoid availability (Blount et al 2003;Grether et al 2004;McGraw & Ardia 2004).…”

Section: Introductionmentioning

confidence: 99%

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Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird ( Turdus merula )

et al. 2007

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Many parasites depress the expression of the carotenoid-based colour displays of their hosts, and it has been hypothesized that animals face a trade-off in carotenoid allocation between immune functions and 'degree of ornamentation'. While numerous correlative studies suggest that parasite infection decreases the intensity of carotenoid-based colour displays, the existence of this trade-off has never been demonstrated experimentally in a host-parasite model. In this study, we used the blackbird (Turdus merula) and Isospora (an intestinal parasite) to assess whether this trade-off does indeed exist. Blackbirds were supplemented with carotenoids while simultaneously being exposed to parasites. Supplemented males circulated more carotenoids in the blood and developed more brightly coloured bills than unsupplemented males. In addition, supplementation slowed down the replication rate of parasites. Supplementation with carotenoids enabled infected birds to maintain their bill coloration, whereas birds that were infected but not supplemented showed reduced bill coloration. At the same time, infection slowed carotenoid assimilation in the blood. Overall, we demonstrated that bill colour reflects a bird's health, and that only males with a carotenoid-rich diet are capable of coping with costs associated with parasitic infection. Carotenoids are thus traded off between host physiological response to parasites and secondary sexual traits. Further investigations are required to determine the physiological mechanisms that govern this trade-off.

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Section: Discussionsupporting

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird ( Turdus merula )

et al. 2007

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“…The carotenoid-based ornaments of birds are particularly sensitive to parasite infections (Lozano, 1994), as demonstrated with a range of diseases and parasites (e.g. Brawner et al, 2000;Hill et al, 2004;Hõrak et al, 2001;Hõrak et al, 2004;Martinez-Padilla et al, 2007), and should also be sensitive to oxidative stress (Alonso Pike et al, 2007a;von Schantz et al, 1999), itself intimately linked with immune function and disease or parasite resistance (Dowling and Simmons, 2009;Hõrak et al, 2007;Romero et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

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

Mougeot

Martínez‐Padilla

Blount

et al. 2010

Journal of Experimental Biology

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It has been drawn to our attention that Fig. 1A,C,D in J. Exp. Biol. 213, 400-407 appears to show the same data as fig 1a,d,e in a paper published by (some of) the same authors in Journal of Evolutionary Biology (Mougeot et al., 2010). The authors wish to clarify the relationship between these two papers and rectify the lack of cross-referencing.Both papers focus on red grouse and are outputs from the same large-scale field manipulation undertaken in 2006. They represent two, very different, stand-alone studies addressing different conceptual issues. The central experimental manipulation of both papers is the drug treatment of birds. The authors felt it was necessary to include background data in each paper to give the reader confidence in the efficacy of the experimental treatment and to allow the reader to better understand and interpret the main results of the papers, which explore very different physiological mechanisms that influence ornamental colouration.For this reason, the treatment effects on parasite burden and comb colouration were presented in both papers, although a different index of comb redness was used vs adjusted R/(G+B) values (Fig. 1C in J . Exp. Biol.)]. Both indices are accurate reflections of comb redness, gave similar results and have been used in previous studies in different contexts to characterize comb colour. Both papers also include the same data on levels of circulating carotenoids [ Fig. 1D in J. Exp. Biol.; fig. 1d in J. Evol. Biol.]. The authors feel the inclusion of these data in both papers can be justified conceptually. In the J. Exp. Biol. paper, the trade-off between the use of carotenoids for colouring ornaments vs dealing with oxidative stress is central to the key question. In the J. Evol. Biol. paper, these data reinforce the argument that carotenoid levels and ornamental colouration covary with corticosterone levels.The reiteration of background data on parasite removal and carotenoid levels does not compromise the uniqueness of each paper. The papers were submitted to, and published by, the respective journals in parallel, and the absence of cross-referencing was an oversight on the part of the authors, who acknowledge that the figure legends should have cited the corresponding paper and that the different indices used for comb redness should have been clarified.Consequently, the text of Fig. 1 in the J. Exp. Biol. paper should have read: ; (E) plasma concentration of malondialdehyde (MDA; nmol ml -1 ) and (F) plasma TAS (total antioxidant status; mmol ml -1 ). White squares: control males; black squares: treated (dosed) males (purged of parasites). Numbers above error bars refer to sample size (number of males).

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“…Carotenoids might act as significant antioxidants in vivo, thus directly linking ornament pigmentation to resistance to oxidative stress, since more pigmented individuals usually circulate more carotenoids (e.g. Blount et al, 2003;Martínez-Padilla et al, 2007;. Male partridges injected with PHA showed a 13% decrease in circulating carotenoids within 24h .…”

Section: Discussionmentioning

confidence: 99%

Carotenoid-based coloration predicts resistance to oxidative damage during immune challenge

Pérez‐Rodríguez

Mougeot

Alonso‐Álvarez

2010

Journal of Experimental Biology

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SUMMARY Many animal ornaments may have evolved as signals advertising the quality of the bearer. The honesty of the information content of these signals would rely on the costs associated with their expression, these being relatively greater for low-quality than for high-quality individuals. Given the physiological functions of carotenoids, carotenoid-based ornaments could indicate individual immunocompetence, and possibly the ability to mount an immune response at a lower cost. We evaluated whether the red carotenoid-based coloration of male red-legged partridges (Alectoris rufa) predicts the capacity of the individual to counteract the oxidative stress generated by a cell-mediated immune response. Individuals were subcutaneously injected with phytohaemagglutinin (PHA) or phosphate buffer solution (PBS) as a control. We found that eye ring pigmentation predicted the change in the amount of peroxidized lipids (TBARS) in blood after the PHA-induced inflammatory challenge. The degree of pigmentation of this carotenoid-based ornament was also negatively related to individual changes in γ-glutamyl transferase (GGT), another biomarker of oxidative stress involved in antioxidant metabolism (i.e. glutathione recycling). However, changes in circulating carotenoids did not significantly explain changes in lipid peroxidation or GGT levels, suggesting that the higher resistance to oxidative stress of those individuals with more pigmented eye rings was not directly mediated by their greater circulating levels of carotenoids. Our results indicate that carotenoid-based coloration can predict not only immune responsiveness (more coloured males mount greater responses) but also an individual's ability to counter the oxidative stress generated during immune challenge (more coloured males experience less oxidative damage when mounting an immune response).

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Nematode parasites reduce carotenoid-based signalling in male red grouse

Cited by 81 publications

References 19 publications

Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird ( Turdus merula )

Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird ( Turdus merula )

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

Carotenoid-based coloration predicts resistance to oxidative damage during immune challenge

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