Age-dependent allocation of carotenoids to colorationversusantioxidant defences

Abstract

SUMMARYAging is commonly attributed to age-related changes in oxidative damage due to an increased production of reactive oxygen species (ROS) and a weakened efficacy of enzymatic antioxidants. These age-related changes might therefore modify the use of dietary antioxidants, including carotenoids. As carotenoids are closely associated with the expression of secondary sexual signals, the allocation of carotenoids to sexual signal versus antioxidant defences may vary with age. In this study, we explored how carotenoid-based ornament and antioxidant activity varied with age and how an inflammatory-induced oxidative burst affected ornament and antioxidant activity across a range of ages. Using zebra finches (Taeniopygia guttata) as a model species, we assessed circulating carotenoids, beak coloration and the plasma antioxidant status of birds of different ages before and after an inflammatory challenge. Our results show that old individuals display similar carotenoid-based sexual signals regardless of the availability of circulating carotenoids, suggesting a terminal investment of old individuals in their last reproductive event. Additionally, we found that an inflammatory insult induced a decrease in the total antioxidant activity and in the expression of a carotenoid-based sexual signal in the oldest individuals. These results suggest that old individuals pay an extra cost of immune activation possibly because the efficiency of antioxidant machinery varies with age.

Is oxidative status influenced by dietary carotenoid and physical activity after moult in the great tit (Parus major)?

“…Carotenoids are known to regulate and stimulate immune function (Hõrak et al, 2004;Biard et al, 2009;Cote et al, 2010;Hill and Johnson, 2012) and to participate in reducing oxidative stress (Surai and Speake, 1998;Blount et al, 2000;Isaksson, 2009). We experimentally investigated the influence of dietary carotenoids on oxidative stress in the great tit after moult, by simultaneously manipulating carotenoid availability and physical activity, the latter being an attempt to increase oxidative stress as a result of an increase in metabolism.…”

“…Moreover, activation of the immune system may induce changes in antioxidant status. For example, immune-challenged nestlings of Falco tinnunculus showed higher ROM concentration and lower antioxidant capacity (Costantini and Dell'Omo, 2006), and in old zebra finches total antioxidant activity decreased more for immune-activated birds than for control birds whereas the opposite pattern was observed for young birds (Cote et al, 2010). The potential signalling function of carotenoid-based coloration with regard to oxidative stress is still unclear.…”

“…Vertebrates cannot produce these molecules, and must acquire them from food (Hill and McGraw, 2006;Isaksson, 2009). In addition to their role in pigmentation, carotenoids have multiple physiological roles Hill and McGraw, 2006) including regulating and stimulating immune function (Hõrak et al, 2004;Biard et al, 2009;Cote et al, 2010;Hill and Johnson, 2012) and participating in maintaining oxidative balance through their antioxidant properties (Surai and Speake, 1998;Blount et al, 2000;Isaksson, 2009).…”

“…Indeed, immune challenge ( parasitism or infection) decreases the brightness of the yellow throat and ventral colour in wall lizards (Martín et al, 2008;López et al, 2009;Calsbeek et al, 2010). Similarly in birds, immune challenge decreases carotenoid-based yellow bill colour in blackbirds (Faivre et al, 2003), red bill colour of zebra finches (Cote et al, 2010) and feather colour of great tit nestlings before fledging (Romero-Diaz et al, 2013). Thus, coloration may be a reliable signal of physiological or immune condition.…”

“…The potential signalling function of carotenoid-based coloration with regard to oxidative stress is still unclear. Indeed, while many studies did not find a significant correlation between oxidative status and coloration (Isaksson et al, 2007b;Isaksson and Andersson, 2008;Cote et al, 2010;Hõrak et al, 2010), others documented a negative correlation between coloration and oxidative damage (Slagsvold and Lifjeld, 1990;Sanz et al, 2000;Leclaire et al, 2011;Patterson et al, 2011) due to the antioxidant activity of carotenoids .…”