Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird

Abstract

In egg-laying animals, mothers can influence the development of their offspring via the suite of biochemicals they incorporate into the nourishing yolk (e.g. lipids, hormones). However, the long-lasting fitness consequences of this early nutritional environment have often proved elusive. Here, we show that the colorful carotenoid pigments that female zebra finches (Taeniopygia guttata) deposit into egg yolks influence embryonic and nestling survival, the sex ratio of fledged offspring, and the eventual ornamental coloration displayed by their offspring as adults. Mothers experimentally supplemented with dietary carotenoids prior to egg-laying incorporated more carotenoids into eggs, which, due to the antioxidant activity of carotenoids, rendered their embryos less susceptible to free-radical attack during development. These eggs were subsequently more likely to hatch, fledge offspring, produce more sons than daughters, and produce sons who exhibited more brightly colored carotenoid-based beak pigmentation. Provisioned mothers also acquired more colorful beaks, which directly predicted levels of carotenoids found in eggs, thus indicating that these pigments may function not only as physiological 'damage-protectants' in adults and offspring but also as morphological signals of maternal reproductive capabilities.

Differential allocation in relation to mate song quality in the Bengalese finch

“…Differential sex allocation has been intensively investigated in model species of songbirds in captivity (notably the zebra finch), where it is easy to experimentally control male physical traits and female conditions. However, evidence for whether or not mothers invest more in sons than daughters under favorable breeding circumstances (e.g., better nutrition or mates) remains controversial especially in the zebra finch (Burley, 1981;Burley, 1986;Kilner, 1998;Rutstein et al, 2004;McGraw et al, 2005;Rutstein et al, 2005b). In addition, laying sequence, which is associated with sibling rivalry resulting from asynchronous hatching, can have confounding effects on differential sex allocation (Rutkowska & Cichoń, 2002;Rutstein et al, 2005a).…”

A window on the past: male ornamental plumage reveals the quality of their early-life environment

“…First, carotenoids provided to nestlings may be stored, for example, in the liver [54], and later deposited in the integument during moult (in this case 1.5-3 months after fledging). Second, individuals with increased access to carotenoids as young birds may have an improved ability to assimilate carotenoids as adults [10]. That we find a correlation between nestling carotenoid concentration and adult plumage colour, but no effect of nestling carotenoid treatment on adult plumage colour, suggests that there is individual variation in nestling response to supplementation.…”

“…Previously, the importance of developmental conditions has been demonstrated for some colourful adult integuments [8,10,20], and for nestling plumage [12,14], but never for adult plumage. The effect was most pronounced for yellow carotenoid-based plumage, which reflected multiple attributes of the nestling environment, such as brood size, hatch date and nutritional conditions.…”

“…It is reasonable to expect a link between developmental environment and colourful traits. The long-term effects of developmental nutrition on morphology, physiology and metabolism can influence adult ability to assimilate the dietary pigments necessary for pigment-based coloration [9,10], and potentially also to form feather nanostructures necessary for structural coloration [11]. A number of studies have considered the immediate effects of developmental environment on nestling plumage colour [12 -15], demonstrating, for example, the importance of maternally invested egg yolk carotenoids for yellow plumage in nestling blue tits [16].…”

Maternally invested carotenoids compensate costly ectoparasitism in the hihi

“…Carotenoids are one such biomolecule invested by breeding females into the egg yolk (14). This maternal investment of carotenoids into eggs has been positively associated with health, vigor, and survival of offspring (12,(15)(16)(17)(18)(19). Of the beneficial roles carotenoids play, their positive actions in the immune system are thought to be of primary importance (20).…”