Interactive effects of yolk testosterone and carotenoid on prenatal growth and offspring physiology in a precocial bird

Abstract

Conditions experienced by individuals during prenatal development can have long-term effects on their phenotype. Maternally transmitted resources are important mediators of such prenatal effects, but the potential interactive effects among them in shaping offspring phenotype have never been studied. Maternally derived testosterone is known to stimulate growth, but these benefits may be counterbalanced by an increase in the production of reactive oxygen species (ROS). Maternally transmitted carotenoids might have the capacity to scavenge ROS and thereby buffer an increase in oxidative stress caused by prenatal exposure to high testosterone levels. Here, we experimentally tested for such interactive effects between maternal yolk testosterone and carotenoid in Japanese quail (Coturnix japonica). We found that hatching mass was reduced and reactive oxygen metabolites (ROMs) levels at the end of the period of maximal growth increased in chicks from eggs injected with either testosterone or carotenoid (only a tendency in chicks from testosterone-injected eggs). However, when both egg compounds were manipulated simultaneously, hatching mass and ROM levels were not affected, showing that both carotenoid and testosterone lose their detrimental effects when the ratio between the 2 compounds is balanced. Our study provides the first experimental evidence for interactive effects of 2 maternally derived egg compounds on offspring phenotype and suggests that developmental cues are tightly coadjusted within an egg. INTERACTIVE EFFECTS OF YOLK TESTOSTERONE AND CAROTENOID ON 10 PRE-NATAL GROWTH AND OFFSPRING PHYSIOLOGY IN A PRECOCIAL BIRD

Co-adjustment of yolk antioxidants and androgens in birds

“…beta-carotene) recycle vitamin E in vitro [14], enhancing the antioxidant potential of vitamin E, we predicted a positive relationship between yolk carotenoids and vitamin E levels. Second, under the hypothesis that antioxidants limit the negative effects of an exposure to high levels of testosterone on oxidative stress levels [3], we also predicted that yolk antioxidant levels should increase with increasing levels of yolk androgens. We tested these predictions in a comparative analysis of the yolk biochemical composition of bird species for which data on yolk antioxidant (i.e.…”

In ovo yolk carotenoid and testosterone levels interactively influence female transfer of yolk antioxidants to her eggs

“…Female Japanese quail that were exposed to high carotenoid levels during embryonic development transferred significantly lower concentrations of yolk antioxidants to their own eggs, but this effect disappeared when both testosterone and carotenoid concentrations were manipulated simultaneously in ovo. We previously showed a similar interactive effect of yolk testosterone and carotenoid manipulation on reactive oxygen metabolite levels at the end of the growth period (5 week-old birds) [8]. Prenatal exposure to high concentrations of yolk carotenoids increased oxidative damage levels at adulthood, but only when yolk testosterone concentrations were not experimentally increased as well, indicating that prenatal conditions (i.e.…”

“…Adult male and female quails were randomly selected from a captive population maintained at the University of Zurich, Switzerland and housed in pairs in cages. Eggs were collected and each clutch was randomly assigned to one of the four treatments: yolk carotenoid (C) manipulation (injection of 15 mg lutein dissolved in 15 ml of safflower oil), yolk testosterone (T) manipulation (15 ng of testosterone), both yolk carotenoid and yolk testosterone (CT) manipulation or a control (CO) injection (injection of 15 ml of safflower oil) (see Giraudeau et al [8] for a full description of the methods). The doses of testosterone and carotenoids injected represent approximately 1 s.d.…”

“…testosterone) and antioxidant (i.e. carotenoids) levels on prenatal growth and juvenile oxidative stress levels in Japanese quail [8] (Coturnix japonica).…”

Matrilineal inheritance of a key mediator of prenatal maternal effects

“…We can exclude that the lack of an effect was due to an unsuccessful manipulation, because the yolk T treatment affected a range of other behavioural and physiological traits in our study [30] as well as in other studies [48,49]. Rather, it suggests that whereas prenatal exposure to T has long-term effects on both circulating T levels and T sensitivity [46,47], it does not affect the transfer of T to the eggs.…”