Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance

Mougeot, François; Martínez‐Padilla, Jesús; Webster, Lucy M.I.; Blount, Jonathan D.; Pérez‐Rodríguez, Lorenzo; Piertney, Stuart B.

doi:10.1098/rspb.2008.1570

Cited by 83 publications

(104 citation statements)

References 40 publications

(76 reference statements)

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“…Consistent with our results, a recent study on red grouse found that the size of a similar carotenoid-based ornament before an experimental parasite infection predicted the magnitude of the subsequent change in parasite-induced oxidative damage (Mougeot et al, 2009a). Again, in red-legged partridges, eye ring coloration also revealed the individual's capacity to endure oxidative challenges in the past, as partridges maintaining redder eye rings at the end of reproduction were also those with less oxidative damage (TBARS) at that time (Alonso-Alvarez et al, 2008).…”

Section: Discussionsupporting

confidence: 81%

“…However, previous studies have reported an increase in oxidative stress associated with a PHA immune challenge (Costantini and Dell'Omo, 2006;Hõrak et al, 2007), supporting the existence of an oxidative cost associated with the cell-mediated immune response (Costantini and Møller, 2009;Sorci and Faivre, 2009). Parasite challenges and infections were also shown to increase oxidative damage in another gallinacean, the red grouse Lagopus lagopus scoticus (Mougeot et al, 2009a;Mougeot et al, 2010), consistent with the idea that raising an immune response increases oxidative stress.…”

Section: Discussionsupporting

confidence: 58%

“…Many experiments have evidenced the production costs of displaying elaborate ornaments, but the relative differences in such costs depending on individual quality have often been overlooked. In fact, much emphasis has been put on treatment level effects to the detriment of analyses of individual responses to treatments (but see Loyau et al, 2005;Dawson and Bortolotti, 2006;Mougeot et al, 2009a;Bortolotti et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 81%

Section: Discussionsupporting

confidence: 58%

Section: Introductionmentioning

confidence: 99%

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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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“…This method has already been described and used successfully in several studies (e.g. Mougeot et al, 2009;Losdat et al, 2011b).…”

Section: Oxidative Damagementioning

confidence: 99%

Differential effects of vitamins E and C and carotenoids on growth, resistance to oxidative stress, fledging success and plumage colouration in wild great tits

Marri

Richner

2014

Journal of Experimental Biology

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Oxidative stress is the imbalance between the production of reactive species and antioxidants, which causes damage to lipids, proteins and DNA. Antioxidants, like vitamins and carotenoids, can limit oxidative damage and can therefore regulate the trade-off between growth, which is a period of high reactive species production, and self-maintenance. However, the role of carotenoids as antioxidants in vivo has been debated, and it has been suggested that carotenoidbased signals indicate the availability of non-pigmentary antioxidants (e.g. vitamins) that protect carotenoids from oxidation, known as the 'protection hypothesis'. To evaluate the importance of vitamins versus carotenoids as antioxidants during growth and to test the protection hypothesis, we supplemented nestling great tits, Parus major, 3, 5 and 7 days after hatching with a single dose of carotenoids and/or vitamins in a 2×2 full-factorial design. We subsequently measured body condition, antioxidant capacity, oxidative damage, fledging success and plumage reflectance. Vitamins enhanced antioxidant capacity, but did not affect oxidative damage. Vitamin-treated nestlings had higher growth rates and higher probability of fledging. In contrast, carotenoids did not affect any of these traits. Furthermore, carotenoid-based colouration increased over the breeding season in nestlings that received vitamins only. This study shows that vitamins are limiting for growth rate and fledging success, and suggests that vitamins could regulate the trade-off between growth and selfmaintenance in favour of the former. Moreover, our results are consistent with the idea that carotenoids are minor antioxidants in birds, but they do not support the protection hypothesis.

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“…This has been shown in lekking species such as black grouse Tetrao tetrix, in which males with bigger combs achieve greater mating success (Rintamaki et al 2000), as well as in monogamous species, such as the rock ptarmigan Lagopus mutus (Bart and Earnst 1999) or the red grouse Mougeot et al 2007Mougeot et al , 2009, in which males with bigger combs hold larger territories, are dominant and preferred by females. A main parasite of red grouse is the nematode Trichostrongylus tenuis, which has well documented negative impacts on this host (Martinez-Padilla et al 2014), reducing condition and comb size in both males (Mougeot et al 2005a(Mougeot et al , 2009 and females (Martinez-Padilla et al 2011). We sampled social pairs on three study sites before laying and reduced T. tenuis parasite abundance in some females using an anthelminthic treatment.…”

Section: Introductionmentioning

confidence: 99%

Parasites, mate attractiveness and female feather corticosterone levels in a socially monogamous bird

Mougeot

Lendvai

Martínez‐Padilla

et al. 2015

Behav Ecol Sociobiol

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Stress is ubiquitous in the life of animals and a key determinant of their well-being and fitness. By quantifying levels of feather corticosterone in growing feathers (CORTf), we measured integrated stress responses in a monogamous game bird, the red grouse Lagopus lagopus scoticus. We investigated the effects of parasites and social mate choice on female CORTf levels during pairing, and tested the hypothesis that females with more parasites and paired with less attractive males have higher CORTf. We experimentally reduced nematode parasite abundance during pairing in females and investigated the effect of treatment on CORTf, while also considering the social mate's phenotype (male comb size, as a proxy of sexual attractiveness). The treatment was effective at contrasting parasite loads between control and dosed females, but had no apparent effect on CORTf. In experimental females, reinfection rate after a month positively correlated with CORTf. We found no evidence of assortative mating based on size, condition or ornament size, but females paired with more attractive males (displaying bigger combs) had lower CORTf during pairing. Females for which parasite load was reduced had lower CORTf than control females at all levels of male attractiveness. Social mate choice therefore appears to be an important determinant of female integrated stress responses, which may in turn modulate reinfection rate and parasitism risk. An influence of male attractiveness on female stress may be part of an adaptive response allowing females to adjust reproductive investment to their achieved social mate choice. Significance statementMate choice is often constrained by the availability of potential mates and not all females socially pair with their preferred partner. We show here that in females of a socially monogamous bird, corticosterone levels in feathers (indicative of integrated stress responses) increase with parasite infection levels but decrease with the attractiveness of the social mate. These results contribute to a better understanding of how females may adjust their reproductive investment according to their achieved mate choice.

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Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance

Cited by 83 publications

References 40 publications

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

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

Differential effects of vitamins E and C and carotenoids on growth, resistance to oxidative stress, fledging success and plumage colouration in wild great tits

Parasites, mate attractiveness and female feather corticosterone levels in a socially monogamous bird

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