Specific carotenoid pigments in the diet and a bit of oxidative stress in the recipe for producing red carotenoid-based signals

Abstract

Colorful ornaments have been the focus of sexual selection studies since the work of Darwin. Yellow to red coloration is often produced by carotenoid pigments. Different hypotheses have been formulated to explain the evolution of these traits as signals of individual quality. Many of these hypotheses involve the existence of a signal production cost. The carotenoids necessary for signaling can only be obtained from food. In this line, carotenoid-based signals could reveal an individual’s capacity to find sufficient dietary pigments. However, the ingested carotenoids are often yellow and became transformed by the organism to produce pigments of more intense color (red ketocarotenoids). Biotransformation should involve oxidation reactions, although the exact mechanism is poorly known. We tested the hypothesis that carotenoid biotransformation could be costly because a certain level of oxidative stress is required to correctly perform the conversion. The carotenoid-based signals could thus reveal the efficiency of the owner in successfully managing this challenge. In a bird with ketocarotenoid-based ornaments (the red-legged partridge; Alectoris rufa), the availability of different carotenoids in the diet (i.e. astaxanthin, zeaxanthin and lutein) and oxidative stress were manipulated. The carotenoid composition was analyzed and quantified in the ornaments, blood, liver and fat. A number of oxidative stress biomarkers were also measured in the same tissues. First, we found that color and pigment levels in the ornaments depended on food levels of those carotenoids used as substrates in biotransformation. Second, we found that birds exposed to mild levels of a free radical generator (diquat) developed redder bills and deposited higher amounts of ketocarotenoids (astaxanthin) in ornaments. Moreover, the same diquat-exposed birds also showed a weaker resistance to hemolysis when their erythrocytes were exposed to free radicals, with females also enduring higher oxidative damage in plasma lipids. Thus, higher color production would be linked to higher oxidative stress, supporting the biotransformation hypothesis. The recent discovery of an avian oxygenase enzyme involved in converting yellow to red carotenoids may support our results. Nonetheless, the effect could also depend on the abundance of specific substrate carotenoids in the diet. Birds fed with proportionally higher levels of zeaxanthin showed the reddest ornaments with the highest astaxanthin concentrations. Moreover, these birds tended to show the strongest diquat-mediated effect. Therefore, in the evolution of carotenoid-based sexual signals, a biotransformation cost derived from maintaining a well-adjusted redox machinery could coexist with a cost linked to carotenoid acquisition and allocation (i.e. a resource allocation trade-off).

Do carotenoid‐based ornaments entail resource trade‐offs? An evaluation of theory and data

“…A recent study by Tomášek et al (2016) has proposed that an important explanation for inconsistency in relationships between carotenoids and oxidative stress is that the current commonly used methods for measuring antioxidant defences fail to capture the effects of carotenoids because they focus on hydrophilic rather than lipophilic reactions (given that carotenoids themselves are lipophilic). García-de Blas et al (2016) also found that hydrophilic antioxidant capacity in red-legged partridges was largely affected by hydrophilic antioxidants rather than lipophilic carotenoids. The implication that the most commonly used methods for estimating antioxidant defences in studies of carotenoid-based coloration in birds are likely to miss effects of carotenoid activity is intriguing and may provide some explanation for the inconsistency of previous studies, although measurement of antioxidant capacity is only one aspect of oxidative stress that has been tested.…”

“…García‐de Blas et al. () also found that hydrophilic antioxidant capacity in red‐legged partridges was largely affected by hydrophilic antioxidants rather than lipophilic carotenoids. The implication that the most commonly used methods for estimating antioxidant defences in studies of carotenoid‐based coloration in birds are likely to miss effects of carotenoid activity is intriguing and may provide some explanation for the inconsistency of previous studies, although measurement of antioxidant capacity is only one aspect of oxidative stress that has been tested.…”

“…Two meta‐analyses have examined relationships between circulating carotenoids and/or carotenoid‐based coloration and oxidative stress parameters and both reported small and generally non‐significant effect sizes (Costantini & Møller, ; Simons et al., ). Others have suggested that carotenoids may indicate oxidative state without directly participating as antioxidants, such as by becoming “bleached” during oxidative stress (Hartley & Kennedy, ) or because only particular oxidative states (García‐de Blas et al., ) or high levels of cellular functionality (Johnson & Hill, ) facilitate the conversion of dietary carotenoids into ornamental carotenoids. While carotenoids are, by their chemical nature, effective electron receivers under most conditions and hence are potential antioxidants (El‐Agamey et al., ; Krinsky & Yeum, ; Stahl & Sies, ), it is uncertain whether the physiological systems of birds are adapted to deploy carotenoids as important antioxidants to maintain redox balance (Perez‐Rodriguez, ).…”

“…For instance, when the red carotenoid canthaxanthin is provided in diet (Hill, 1992), birds can bypass the oxidation of yellow pigments to red (Lopes et al, 2016). More subtle changes in the ratio of carotenoids in supplemented diets-such as the ratio of lutein to zeaxanthin-can further alter the effects of supplementation (Fitze, Tschirren, Gasparini, & Richner, 2007;García-de Blas, Mateo, & Alonso-Alvarez, 2016). Experimental supplementation may therefore provide different quantities of various carotenoids at artificially high relative abundances and for different periods of time than what any bird would experience in the wild (Koch, Wilson, & Hill, 2015), which makes it difficult to assess the relevance of results of supplementation to variation observed in wild populations.…”

Ecologia da interação parasito-hospedeiro: efeitos da malária sobre a coloração de carotenoides na plumagem e condição corporal de aves em área de Cerrado

“…Os ornamentos vermelhos são, em geral, resultados da biotransformação do hidrocarotenoide amarelo em keto-carotenoide vermelho (McGraw, 2006). Esse processo requer reações de hidrogenação e oxidação (de Blas et al, 2016). O status oxidativo dos indivíduos de aves influencia na atividade de enzimas responsáveis por processos oxidativos e de hidrogenação, indicando a capacidade do indivíduo em lidar com o estresse oxidativo, ligado à transformação de carotenoides (Johnson & Hill, 2013).…”