Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring.

Organisms frequently encounter stressful ecological conditions. In vertebrates, a major mechanism of physiological response to stress is mediated by the hypothalamic-pituitary-adrenal axis and results in increased secretion of glucocorticosteroids, which can have adverse consequences on diverse phenotypic traits affecting fitness. Maternal stress may thus have carry-over effects on progeny if it influences pre-natal offspring environment in terms of glucocorticosteroid concentration, although this hypothesis has never been tested in any species under field conditions. We manipulated stress experienced by female barn swallows Hirundo rustica, by exposing them to a predator during laying and measured egg corticosterone concentration. Stressed females laid eggs with greater corticosterone concentration than controls exposed to a herbivore. In another experiment, we injected physiological doses of corticosterone in the egg albumen and compared the phenotype of offspring originating from these eggs with their control siblings originating from either sham-inoculated or unmanipulated eggs and reared in the same nest. Eggs injected with corticosterone had lower hatchability and produced fledglings with smaller body size and slower plumage development than did control eggs. Nestling body size in our study population predicts long-term survival. Thus, maternal stress impaired offspring phenotype and viability by increasing transmission of glucocorticosteroids to the eggs. This study identifies a novel mechanism mediating early maternal effects whereby maternal stress affects offspring quality. These results are relevant to biological conservation because they disclose a mechanism that can link environmental conditions to population productivity and viability.

Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks.

Eggs of vertebrates contain steroid hormones of maternal origin that may influence offspring performance. Recently, it has been shown that glucocorticoids, which are the main hormones mediating the stress response in vertebrates, are transmitted from the mother to the egg in birds. In addition, mothers with experimentally elevated corticosterone levels lay eggs with larger concentrations of the hormone, which produce slow growing offspring with high activity of the hypothalamo-adrenal axis under acute stress. However, the effects and function of transfer of maternal corticosterone to the eggs are largely unknown. In the present study, we injected corticosterone in freshly laid eggs of yellow-legged gulls (Larus michahellis), thus increasing the concentration of the hormone within its natural range of variation, and analyzed the effect of manipulation on behavioral, morphological, and immune traits of the offspring in the wild. Eggs injected with corticosterone had similar hatching success to controls, but hatched later. Mass loss during incubation was greater for corticosterone-treated eggs, except for the last laid ones. Corticosterone injection reduced rate and loudness of late embryonic vocalizations and the intensity of chick begging display. Tonic immobility response, reflecting innate fearfulness, was unaffected by hormone treatment. Elevated egg corticosterone concentrations depressed T-cell-mediated immunity but had no detectable effects on humoral immune response to a novel antigen, viability at day 10, or growth. Present results suggest that egg corticosterone can affect the behavior and immunity of offspring in birds and disclose a mechanism mediating early maternal effects whereby stress experienced by females may negatively translate to offspring phenotypic quality.

Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation.

Carotenoids are critical to embryonic development, immunity and protection from oxidative stress. Transmission of carotenoids to the eggs may affect development and maturation of immunity in offspring, but carotenoids may be available to females in limiting amounts. Females may thus transfer carotenoids to the eggs differentially in relation to the reproductive value of the offspring as affected by sexual ornamentation of their father. In this study of maternal allocation of carotenoids to the eggs in the barn swallow (Hirundo rustica), females whose immune system had been experimentally challenged with an antigen had smaller lutein concentrations in their eggs than controls. We manipulated the size of a secondary sexual character (tail length) of males, and analysed the effect of manipulation on allocation of lutein to eggs by their vaccinated mates. Contrary to our prediction based on parental allocation theory, mates of tail-shortened males had a larger lutein concentration in their eggs compared with those of control and tail-elongated males. According to previous studies, offspring of short-tailed males have larger exposure and/or susceptibility to parasites. A larger lutein concentration in the eggs of females mated to males with experimentally reduced ornaments may thus reflect adaptive maternal strategies to enhance offspring viability.

Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner.

Vertebrates have an immature immune system soon after birth, and parasites can therefore be particularly virulent to young hosts. Transfer of immune factors via the egg can give rise to early maternal effects with important consequences for offspring fitness, as maternally derived immunity confers anti-parasite protection. Mothers are expected to allocate immunity differentially to the eggs according to the reproductive value of their offspring as influenced by the quality of their father. In this study, we analysed transmission to the yolk of antibodies specific to an antigen (Newcastle disease virus vaccine, NDV) by vaccinated female barn swallows (Hirundo rustica) mated to males whose secondary sexual characteristics had been manipulated. Concentration of anti-NDV antibodies in the yolk positively covaried with that in maternal plasma. Anti-NDV antibodies were more concentrated in the first but not the fourth eggs laid by females mated with tail-elongated males compared with those mated with tail-shortened and control males. This experiment shows that allocation of maternal immune factors to the eggs is affected by quality of the male, as signalled by its secondary sexual characteristic. Thus, early maternal effects are influenced by sexual attractiveness of male mates and are mediated by immunity.