Carotenoids in evolutionary ecology: re‐evaluating the antioxidant role

Abstract

The antioxidant role of carotenoids in the living organism was proposed as a possible basis for the honesty of carotenoid-based signals. However, recent studies have questioned the relevance of carotenoids as powerful antioxidants in vivo. Current evidence does not seem to support the "antioxidant role" hypothesis, but it does not allow us to reject it either. This paper proposes some steps to solve this controversy, such as taking a dynamic approach to antioxidant responses, designing protocols that expose individuals to oxidative challenges, analyzing tissues other than blood, and obtaining measures of antioxidant capacity and oxidative damage simultaneously. However, it should be considered that, irrespective of their antioxidant potential, carotenoids might still give information on oxidative stress levels if they are particularly sensitive to free radicals. Finally, lumping together the immunostimulatory and antioxidant roles of carotenoids should be avoided as these functions are not necessarily associated.

On the methodological limitations of detecting oxidative stress: effects of paraquat on measures of oxidative status in greenfinches

“…Another experiment manipulating oxidative status in greenfinches by blocking the synthesis of GSH also failed to detect any effects on circulating carotenoids or carotenoid-based feather colouration, although plasma MDA levels were increased . These findings are consistent with the idea that circulating carotenoids do not contribute much to the antioxidant defences of birds (Hartley and Kennedy, 2004;Costantini and Møller, 2008;Pérez-Rodríguez, 2009). However, administration of a related pro-oxidant, diquat, to growing red-legged partridges (0.5mll -1 for 33days) reduced plasma carotenoid levels and allocation of carotenoids into red beaks and eye rings (AlonsoAlvarez and Galván, 2011).…”

“…Pérez-Rodríguez, 2009;Hõrak and Cohen, 2010). We are currently aware of only a few similar experiments, performed in wild bird species.…”

Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irradiation and enhances male sexual performance in the Caribbean fruit fly, Anastrepha suspensa

“…However, antioxidant-boosting anoxic conditioning did not enhance any metric of performance in unstressed individuals, an observation that is consistent with physiological conditioning hormesis. Higher antioxidant levels have been associated with greater mating competitiveness and sexual selection in numerous taxa (Peters et al, 2004;Catoni et al, 2008;Pérez-Rodríguez, 2009;Costantini et al, 2010a;Metcalfe and Alonzo-Alvarez, 2010), although this work has typically focused on diet-derived carotenoids rather than endogenous antioxidants. Caribflies have a highly competitive lek-mating system with strong potential for sexual selection on male condition (Dodson, 1982;Burk, 1984;Sivinski, 1989;Pereira et al, 2010), so oxidative stress is expected to be deleterious to male mating success.…”

Carotenoid intake does not affect immune-stimulated oxidative burst in greenfinches

“…Although vertebrates cannot synthesise carotenoids de novo, these pigments are common components of the colour of signals used in mate attraction and other types of social communication (Blount and McGraw, 2008;Møller et al, 2000;Pérez-Rodríguez, 2009;Svensson and Wong, 2011). The question about what qualities animals communicate by these pigments rose into the focus of physiological ecologists after recognizing the potential health impact of carotenoids.…”

“…Accordingly, carotenoid-based ornaments enable individuals to signal their past and/or current health state; carotenoids can be allocated to signalling only if and when they are not needed for other purposes at the same time. Recently, however, the direct connection between the antioxidant properties of carotenoids and colouration has been debated (Costantini and Møller, 2008;Hartley and Kennedy, 2004;Pérez-Rodríguez, 2009 Sepp et al, 2011). One of the reasons for this inconsistency may lay in the tight interconnections between the immune and antioxidant systems and the potential ability of carotenoids to quench reactive oxygen species (ROS) (Svensson and Wong, 2011).…”