Prenatal independent and combined effects of yolk vitamin E and corticosterone on embryo growth and oxidative status in the yellow-legged gull

Abstract

Variation in the concentration of antioxidants and hormones of maternal origin in the eggs of birds can have a profound influence on offspring phenotype both prenatally and postnatally. Egg maternal substances can have interacting effects, but experimental studies of the consequences of the combined variation in the egg concentration of such molecules are extremely rare, particularly as far as prenatal stages are concerned. We manipulated the yolk concentration of vitamin E and corticosterone, which are, respectively, the main antioxidant and the main glucocorticoid hormone in bird eggs, both independently and simultaneously, and we tested their separate and combined effects on growth and oxidative status in the liver and in the brain of yellow-legged gull (Larus michahellis) embryos. Egg supplementation of relatively large physiological doses of corticosterone depressed embryo growth (total body mass, tarsus length and liver mass), whereas administration of vitamin E in association with corticosterone restored normal growth. Vitamin E did not affect embryo growth when administered alone. We further analysed the independent and combined effects of vitamin E and corticosterone on liver and brain total antioxidant capacity, the concentration of reactive oxygen molecules and lipid peroxidation. Vitamin E significantly reduced liver total antioxidant capacity, while corticosterone depressed brain lipid peroxidation. Prenatal exposure to vitamin E and corticosterone appears to have antagonistic effects on body growth, although vitamin E is not limiting in yellow-legged gull eggs. In combination with the results of previous experiments on the same species applying smaller experimental doses or focusing on the postnatal rather than prenatal life stages, our findings indicate that the effects of a physiological increase in the egg concentration of these substances can be life stage and dose specific, implying that generalizing prenatal effects of egg compounds may not be feasible.

Natural variation in yolk fatty acids, but not androgens, predicts offspring fitness in a wild bird

“…But when both components were administered together, neither hatchling mass nor oxidative stress were affected. Similar compensatory effects were found in yellow-legged gulls (Larus michahellis) after eggs were simultaneously injected with corticosterone and vitamin E [36,37]. Such studies suggest that the consequences of maternal effects on offspring phenotype known from studies that focus on single components might actually be absent, weakened or potentiated if the presence and actions of other components are also considered.…”

“…This approach has been pivotal for advancing our knowledge of how mothers affect offspring phenotype. However, maternal effects are by nature multivariate (reviewed by [33,34]), with different groups of yolk components influencing similar nestling traits, i.e., by having interactive effects on offspring phenotype [35][36][37]. For instance, hatchling mass was reduced and oxidative stress increased in Japanese quails (Coturnix japonica) hatching from eggs injected with either testosterone or carotenoids [35].…”

Sex ratios and the city: Secondary offspring sex ratios, parental corticosterone, and parental body condition in an urban-adapted bird

“…Mothers are thought to bias their primary sex ratio through CORT and other steroid hormones deposited into the yolk and albumen of the egg (Schwabl, 1993;Engelhardt and Groothuis, 2005;Downing and Bryden, 2008;Navara and Pinson, 2010). Maternal CORT can also significantly impact embryo and nestling development and survival after laying to alter the secondary sex ratio and match offspring needs with maternal care quality (Hayward and Wingfield, 2004;Rubolini et al, 2005;Saino et al, 2005;Schoech et al, 2011;Bowers et al, 2016;Strange et al, 2016;Tilgar et al, 2016;Parolini et al, 2019). Elevated maternal CORT can cause primary sex ratio biases within a season (Love et al, 2005;Bonier et al, 2007), but the relationship between secondary sex ratios and maternal CORT is more complicated (Riechert et al, 2013;Henderson et al, 2014).…”