Abstract
BackgroundCarotenoids can confer somatic and reproductive benefits, but most evidence is from captive animal experimentation or single time-point sampling. Another perhaps more informative means by which to assess physiological contributions to animal performance is by tracking an individual's ability to increase or sustain carotenoids or other health-related molecules over time, as these are likely to be temporally variable.Methodology/Principal Findings In a field study of North American barn swallows (Hirundo rustica erythrogaster), we analyzed within-individual changes in carotenoid concentrations by repeatedly sampling the carotenoid profiles of individuals over the course of the breeding season. Our results demonstrate that carotenoid concentrations of individuals are temporally dynamic and that season-long balance of these molecules, rather than single time-point samples, predict reproductive performance. This was true even when controlling for two important variables associated with reproductive outcomes: (1) timing of breeding and (2) sexually selected plumage coloration, which is itself positively correlated with and concomitantly changes with circulating carotenoid concentrations.Conclusions/SignificanceWhile reproduction itself is purported to impose health stress on organisms, these data suggest that free-ranging, high-quality individuals can mitigate such costs, by one or several genetic, environmental (diet), or physiological mechanisms. Moreover, the temporal variations in both health-linked physiological measures and morphological traits we uncover here merit further examination in other species, especially when goals include the estimation of signal information content or the costs of trait expression.
Highlights
Current research on carotenoids suggests that these molecules can improve health in a variety of animals, including humans [1,2]
Three carotenoid pigments were detected in plasma–lutein, zeaxanthin, and b-cryptoxanthin–all of which we previously reported in the egg yolks of barn swallows [20]
In our longitudinal field study of carotenoid circulation and breeding in barn swallows, we found that single-time-point estimates of carotenoid concentration were not significantly correlated with reproductive performance
Summary
Current research on carotenoids suggests that these molecules can improve health in a variety of animals, including humans [1,2]. Other studies suggest that circulating carotenoids are important underpinnings of condition-dependent signals related to mate-selection and competitive ability [7,8] Many of these results have been obtained from animals in captive situations, where researchers have limited ability to assess the evolutionary and ecological context in which these molecules are linked to survival and reproduction. Previous analyses of carotenoids have relied on point-sampling methods whereas it is likely–though unknown–that an individual’s carotenoid profile in nature is temporally dynamic, as circulating concentrations respond to daily nutritional supplies and to physiological demands for combating oxidative crises [9,10,11] While these molecules certainly can be traded-off between somatic and reproductive functions [10,12,13,14], the degree to which individuals sustain circulating carotenoid supplies and how these affect reproductive performance are unknown. Sexually-selected plumage coloration appears to be temporally related to changes in carotenoids: ventral color appeared to change concomitantly with circulating carotenoid concentrations
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