Antioxidant Defenses Predict Long-Term Survival in a Passerine Bird

Abstract

BackgroundNormal and pathological processes entail the production of oxidative substances that can damage biological molecules and harm physiological functions. Organisms have evolved complex mechanisms of antioxidant defense, and any imbalance between oxidative challenge and antioxidant protection can depress fitness components and accelerate senescence. While the role of oxidative stress in pathogenesis and aging has been studied intensively in humans and model animal species under laboratory conditions, there is a dearth of knowledge on its role in shaping life-histories of animals under natural selection regimes. Yet, given the pervasive nature and likely fitness consequences of oxidative damage, it can be expected that the need to secure efficient antioxidant protection is powerful in molding the evolutionary ecology of animals. Here, we test whether overall antioxidant defense varies with age and predicts long-term survival, using a wild population of a migratory passerine bird, the barn swallow (Hirundo rustica), as a model.Methodology/Principal FindingsPlasma antioxidant capacity (AOC) of breeding individuals was measured using standard protocols and annual survival was monitored over five years (2006–2010) on a large sample of selection episodes. AOC did not covary with age in longitudinal analyses after discounting the effect of selection. AOC positively predicted annual survival independently of sex. Individuals were highly consistent in their relative levels of AOC, implying the existence of additive genetic variance and/or environmental (including early maternal) components consistently acting through their lives.ConclusionsUsing longitudinal data we showed that high levels of antioxidant protection positively predict long-term survival in a wild animal population. Present results are therefore novel in disclosing a role for antioxidant protection in determining survival under natural conditions, strongly demanding for more longitudinal eco-physiological studies of life-histories in relation to oxidative stress in wild populations.

Increased brood size leads to persistent eroded telomeres

“…Such an observation between oxidative damage and survival rate was observed in European shags (Phalacrocorax aristotelis) (Noguera et al, 2012). Antioxidant levels or cell resistance to oxidative stress have also been linked to annual survival rate in free-living barn swallows (Hirundo rustica) (Saino et al, 2011) and male alpine swifts (Apus melba; Bize et al, 2008) respectively, suggesting as well an important role of oxidative balance in immediate individual fitness modulation.…”

Darker eggshell spotting indicates lower yolk antioxidant level and poorer female quality in the Eurasian Great Tit (Parus major)

“…Plasma oxidative status may have changed during this time (Sepp et al 2012), although some studies have demonstrated significant repeatability of the values of OXY and ROM within the same breeding season (Costantini et al 2007, Saino et al 2011.…”

Early life experience primes resistance to oxidative stress

“…Although the phenotype is programmed to deal with a wide range of temperatures, its capacity to cope with unpredictable very high temperatures is likely to have significant fitness consequences. Furthermore, the oxidative stress that may arise as a result of heat stress is likely to be a key mediator in determining the fitness of organisms in the wild, given that the resultant tissue degradation might influence reproductive performance, growth patterns, cellular senescence and survival (Alonso-Alvarez et al, 2006;Costantini and Dell'Omo, 2006;Costantini, 2008;Monaghan et al, 2009;Saino et al, 2011).…”